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 »
- Authors:
-
- Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Illinois, Chicago, IL (United States)
- Univ. of Alabama in Huntsville, Huntsville, AL (United States)
- Argonne National Lab. (ANL), Argonne, IL (United States)
- 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}
}
Web of Science
Works referenced in this record:
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
Gene Ontology: tool for the unification of biology
journal, May 2000
- Ashburner, Michael; Ball, Catherine A.; Blake, Judith A.
- Nature Genetics, Vol. 25, Issue 1
Identification of the Auxin-responsive Element, AuxRE, in the Primary indoleacetic Acid-inducible Gene, PS-IAA4/5, of Pea (Pisum sativum)
journal, October 1993
- Ballas, Nurit; Wong, Lu-Min; Theologis, Athanasios
- Journal of Molecular Biology, Vol. 233, Issue 4
Role of plant hormones in plant defence responses
journal, December 2008
- Bari, Rajendra; Jones, Jonathan D. G.
- Plant Molecular Biology, Vol. 69, Issue 4
Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate
journal, July 2010
- Beer, C.; Reichstein, M.; Tomelleri, E.
- Science, Vol. 329, Issue 5993
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis
journal, July 2010
- Bonfante, Paola; Genre, Andrea
- Nature Communications, Vol. 1, Issue 1
Oxylipins in fungi: Fungal oxylipins
journal, February 2011
- Brodhun, Florian; Feussner, Ivo
- FEBS Journal, Vol. 278, Issue 7
Rank-based edge reconstruction for scale-free genetic regulatory networks
journal, January 2008
- Chen, Guanrao; Larsen, Peter; Almasri, Eyad
- BMC Bioinformatics, Vol. 9, Issue 1
trans meets cis in MADS science
journal, May 2006
- Folter, Stefan de; Angenent, Gerco C.
- Trends in Plant Science, Vol. 11, Issue 5
Plant lectins: the ties that bind in root symbiosis and plant defense
journal, June 2009
- De Hoff, Peter L.; Brill, Laurence M.; Hirsch, Ann M.
- Molecular Genetics and Genomics, Vol. 282, Issue 1
Mutation of either G box or I box sequences profoundly affects expression from the Arabidopsis rbcS-1A promoter.
journal, June 1990
- Donald, R. G.; Cashmore, A. R.
- The EMBO Journal, Vol. 9, Issue 6
Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2
journal, June 2010
- Drigo, B.; Pijl, A. S.; Duyts, H.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 24
The Ectomycorrhizal Fungus Laccaria bicolor Stimulates Lateral Root Formation in Poplar and Arabidopsis through Auxin Transport and Signaling
journal, October 2009
- Felten, Judith; Kohler, Annegret; Morin, Emmanuelle
- Plant Physiology, Vol. 151, Issue 4
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
Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure
journal, April 2005
- Gamper, Hannes; Hartwig, Ueli A.; Leuchtmann, Adrian
- New Phytologist, Vol. 167, Issue 2
Studies on Scaffold Attachment Sites and Their Relation to Genome Function
book, January 1990
- Gasser, S. M.; Amati, B. B.; Cardenas, M. E.
- International Review of Cytology
Promotion of Plant Growth by Bacterial ACC Deaminase
journal, October 2007
- Glick, Bernard R.; Todorovic, Biljana; Czarny, Jennifer
- Critical Reviews in Plant Sciences, Vol. 26, Issue 5-6
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
cis -Regulatory Elements for Mesophyll-Specific Gene Expression in the C 4 Plant Flaveria trinervia , the Promoter of the C 4 Phosphoenolpyruvate Carboxylase Gene
journal, April 2004
- Gowik, Udo; Burscheidt, Janet; Akyildiz, Meryem
- The Plant Cell, Vol. 16, Issue 5
Transcriptome responses to aluminum stress in roots of aspen (Populus tremula)
journal, January 2010
- Grisel, Nadine; Zoller, Stefan; Künzli-Gontarczyk, Marzanna
- BMC Plant Biology, Vol. 10, Issue 1
Combinatorial Interaction of Cis Elements Specifies the Expression of the Arabidopsis AtHsp90-1 Gene
journal, July 2002
- Haralampidis, Kosmas; Milioni, Dimitra; Rigas, Stamatis
- Plant Physiology, Vol. 129, Issue 3
Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs
journal, August 2002
- Hepworth, S. R.
- The EMBO Journal, Vol. 21, Issue 16
Plant cis-acting regulatory DNA elements (PLACE) database: 1999
journal, January 1999
- Higo, K.; Ugawa, Y.; Iwamoto, M.
- Nucleic Acids Research, Vol. 27, Issue 1
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
WoLF PSORT: protein localization predictor
journal, May 2007
- Horton, P.; Park, K. -J.; Obayashi, T.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Plant Immunity to Insect Herbivores
journal, June 2008
- Howe, Gregg A.; Jander, Georg
- Annual Review of Plant Biology, Vol. 59, Issue 1
Isolation of tobacco ubiquitin‐conjugating enzyme cDNA in a yeast two‐hybrid system with tobacco ERF3 as bait and its characterization of specific interaction
journal, April 2003
- Koyama, Tomotsugu; Okada, Takashi; Kitajima, Sakihito
- Journal of Experimental Botany, Vol. 54, Issue 385
Nucleocytoplasmic plant lectins
journal, February 2010
- Lannoo, Nausicaä; Van Damme, Els J. M.
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1800, Issue 2
A statistical method to incorporate biological knowledge for generating testable novel gene regulatory interactions from microarray experiments
journal, January 2007
- Larsen, Peter; Almasri, Eyad; Chen, Guanrao
- BMC Bioinformatics, Vol. 8, Issue 1
Incorporating Network Topology Improves Prediction of Protein Interaction Networks from Transcriptomic Data
journal, July 2010
- Larsen, Peter E.; Collart, Frank; Dai, Yang
- International Journal of Knowledge Discovery in Bioinformatics, Vol. 1, Issue 3
BowStrap v1.0: Assigning statistical significance to expressed genes using short-read transcriptome data
journal, June 2012
- Larsen, Peter E.; Collart, Frank R.
- BMC Research Notes, Vol. 5, Issue 1
Predicted Relative Metabolomic Turnover (PRMT): determining metabolic turnover from a coastal marine metagenomic dataset
journal, June 2011
- Larsen, Peter E.; Collart, Frank R.; Field, Dawn
- Microbial Informatics and Experimentation, Vol. 1, Issue 1
Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome
journal, January 2011
- Larsen, Peter E.; Sreedasyam, Avinash; Trivedi, Geetika
- BMC Systems Biology, Vol. 5, Issue 1
Using Deep RNA Sequencing for the Structural Annotation of the Laccaria Bicolor Mycorrhizal Transcriptome
journal, July 2010
- Larsen, Peter E.; Trivedi, Geetika; Sreedasyam, Avinash
- PLoS ONE, Vol. 5, Issue 7
Up-Regulation of OsBIHD1, a Rice Gene Encoding BELL Homeodomain Transcriptional Factor, in Disease Resistance Responses
journal, September 2005
- Luo, H.; Song, F.; Goodman, R. M.
- Plant Biology, Vol. 7, Issue 5
The Laccaria genome: a symbiont blueprint decoded
journal, October 2008
- Martin, Francis; Selosse, Marc-André
- New Phytologist, Vol. 180, Issue 2
AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization: AGL24 acts as a promoter of flowering in Arabidopsis
journal, February 2003
- Michaels, Scott D.; Ditta, Gary; Gustafson-Brown, Cindy
- The Plant Journal, Vol. 33, Issue 5
Mapping and quantifying mammalian transcriptomes by RNA-Seq
journal, May 2008
- Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth
- Nature Methods, Vol. 5, Issue 7, p. 621-628
Mastering ectomycorrhizal symbiosis: the impact of carbohydrates
journal, February 2008
- Nehls, U.
- Journal of Experimental Botany, Vol. 59, Issue 5
KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 1999
- Ogata, H.; Goto, S.; Sato, K.
- Nucleic Acids Research, Vol. 27, Issue 1
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
Unraveling mycorrhiza-induced resistance
journal, August 2007
- Pozo, María J.; Azcón-Aguilar, Concepción
- Current Opinion in Plant Biology, Vol. 10, Issue 4
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
Activation of the Oryza sativa non-symbiotic haemoglobin-2 promoter by the cytokinin-regulated transcription factor, ARR1
journal, July 2004
- Ross, E. J. H.
- Journal of Experimental Botany, Vol. 55, Issue 403
Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes.
journal, October 1996
- Rushton, P. J.; Torres, J. T.; Parniske, M.
- The EMBO Journal, Vol. 15, Issue 20
TM4: A Free, Open-Source System for Microarray Data Management and Analysis
journal, February 2003
- Saeed, A. I.; Sharov, V.; White, J.
- BioTechniques, Vol. 34, Issue 2
Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators
journal, December 2000
- Sakai, Hiroe; Aoyama, Takashi; Oka, Atsuhiro
- The Plant Journal, Vol. 24, Issue 6
Mycorrhizal Fungi
journal, January 1974
- Smith, S. E.
- CRC Critical Reviews in Microbiology, Vol. 3, Issue 3
Mycorrhizal Fungi Can Dominate Phosphate Supply to Plants Irrespective of Growth Responses
journal, September 2003
- Smith, Sally E.; Smith, F. Andrew; Jakobsen, Iver
- Plant Physiology, Vol. 133, Issue 1
Molecular genetics of plant disease resistance
journal, May 1995
- Staskawicz, B.; Ausubel, F.; Baker, B.
- Science, Vol. 268, Issue 5211
Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions: Auxin, plant roots and plant-microbe interaction
journal, December 2012
- Sukumar, Poornima; LeguÉ, ValÉRie; VayssiÈRes, Alice
- Plant, Cell & Environment, Vol. 36, Issue 5
Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation
journal, June 2006
- Sun, Jongho; Cardoza, Vinitha; Mitchell, David M.
- The Plant Journal, Vol. 46, Issue 6
Light-Regulated Transcription
journal, June 1995
- Terzaghi, William B.; Cashmore, Anthony R.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 46, Issue 1
Evolution of jasmonate and salicylate signal crosstalk
journal, May 2012
- Thaler, Jennifer S.; Humphrey, Parris T.; Whiteman, Noah K.
- Trends in Plant Science, Vol. 17, Issue 5
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.
journal, November 1997
- Ulmasov, T.; Murfett, J.; Hagen, G.
- The Plant Cell, Vol. 9, Issue 11
Inhibition of shoot branching by new terpenoid plant hormones
journal, August 2008
- Umehara, Mikihisa; Hanada, Atsushi; Yoshida, Satoko
- Nature, Vol. 455, Issue 7210
Novel Concepts About the Role of Lectins in the Plant Cell
book, January 2011
- Van Dammes, Els J. M.; Fouquaert, Elke; Lannoo, Nausicaä
- The Molecular Immunology of Complex Carbohydrates-3
Genome-Wide Identification of Potential Plant E2F Target Genes
journal, August 2005
- Vandepoele, Klaas; Vlieghe, Kobe; Florquin, Kobe
- Plant Physiology, Vol. 139, Issue 1
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
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
Identification of the Auxin-responsive Element, AuxRE, in the Primary indoleacetic Acid-inducible Gene, PS-IAA4/5, of Pea (Pisum sativum)
journal, October 1993
- Ballas, Nurit; Wong, Lu-Min; Theologis, Athanasios
- Journal of Molecular Biology, Vol. 233, Issue 4
Organization and expression of the genes encoding ribulose-1,5-bisphosphate carboxylase in higher plants
journal, January 1988
- Manzara, Thianda; Gruissem, Wilhelm
- Photosynthesis Research, Vol. 16, Issue 1-2
A 20 nucleotide upstream element is essential for the nopaline synthase (nos) promoter activity
journal, January 1994
- Kim, Younghee; Buckley, Kimberly; Costa, Michael A.
- Plant Molecular Biology, Vol. 24, Issue 1
Fungal elicitor-mediated responses in pine cell cultures: I. Induction of phenylpropanoid metabolism
journal, February 1992
- Campbell, MalcolmM.; Ellis, BrianE.
- Planta, Vol. 186, Issue 3
Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimaeric heat shock genes in transgenic tobacco
journal, January 1992
- Rieping, Mechthild; Schöffl, Fritz
- Molecular and General Genetics MGG, Vol. 231, Issue 2
Sequences responsible for the tissue specific promoter activity of a pea legumin gene in tobacco
journal, January 1989
- Shirsat, Anil; Wilford, Neville; Croy, Ronald
- Molecular and General Genetics MGG, Vol. 215, Issue 2
Plant lectins: the ties that bind in root symbiosis and plant defense
journal, June 2009
- De Hoff, Peter L.; Brill, Laurence M.; Hirsch, Ann M.
- Molecular Genetics and Genomics, Vol. 282, Issue 1
Role of plant hormones in plant defence responses
journal, December 2008
- Bari, Rajendra; Jones, Jonathan D. G.
- Plant Molecular Biology, Vol. 69, Issue 4
Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation
journal, November 1990
- Clos, Joachim; Westwood, J. Timothy; Becker, Peter B.
- Cell, Vol. 63, Issue 5
Nucleocytoplasmic plant lectins
journal, February 2010
- Lannoo, Nausicaä; Van Damme, Els J. M.
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1800, Issue 2
Unraveling mycorrhiza-induced resistance
journal, August 2007
- Pozo, María J.; Azcón-Aguilar, Concepción
- Current Opinion in Plant Biology, Vol. 10, Issue 4
trans meets cis in MADS science
journal, May 2006
- Folter, Stefan de; Angenent, Gerco C.
- Trends in Plant Science, Vol. 11, Issue 5
Evolution of jasmonate and salicylate signal crosstalk
journal, May 2012
- Thaler, Jennifer S.; Humphrey, Parris T.; Whiteman, Noah K.
- Trends in Plant Science, Vol. 17, Issue 5
Interplay of signaling pathways in plant disease resistance
journal, October 2000
- Feys, Bart J.; Parker, Jane E.
- Trends in Genetics, Vol. 16, Issue 10
Cloning and characterization of a symbiosis-related gene from an ectomycorrhizal fungus Laccaria bicolor
journal, November 1998
- Kim, Sung-Jae; Zheng, Jun; Hiremath, Shivanand T.
- Gene, Vol. 222, Issue 2
The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals
journal, March 1998
- van der Biezen, Erik A.; Jones, Jonathan D. G.
- Current Biology, Vol. 8, Issue 7
The WRKY superfamily of plant transcription factors
journal, May 2000
- Eulgem, Thomas; Rushton, Paul J.; Robatzek, Silke
- Trends in Plant Science, Vol. 5, Issue 5, p. 199-206
The identification of inducible cytoplasmic/nuclear carbohydrate-binding proteins urges to develop novel concepts about the role of plant lectins
journal, January 2003
- Van Damme, Els J. M.; Lannoo, Nausicaä; Fouquaert, Elke
- Glycoconjugate Journal, Vol. 20, Issue 7/8
Inhibition of shoot branching by new terpenoid plant hormones
journal, August 2008
- Umehara, Mikihisa; Hanada, Atsushi; Yoshida, Satoko
- Nature, Vol. 455, Issue 7210
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis
journal, July 2010
- Bonfante, Paola; Genre, Andrea
- Nature Communications, Vol. 1, Issue 1
CCL5 derived from tumor-associated macrophages promotes prostate cancer stem cells and metastasis via activating β-catenin/STAT3 signaling
journal, April 2020
- Huang, Renlun; Wang, Shengqi; Wang, Neng
- Cell Death & Disease, Vol. 11, Issue 4
Dietary palmitic acid promotes a prometastatic memory via Schwann cells
journal, November 2021
- Pascual, Gloria; Domínguez, Diana; Elosúa-Bayes, Marc
- Nature, Vol. 599, Issue 7885
Separate cis sequences and trans factors direct metabolic and developmental regulation of a potato tuber storage protein gene
journal, June 1994
- Grierson, Claire; Du, Jian-Sheng; de Torres Zabala, Marta
- The Plant Journal, Vol. 5, Issue 6
Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators
journal, December 2000
- Sakai, Hiroe; Aoyama, Takashi; Oka, Atsuhiro
- The Plant Journal, Vol. 24, Issue 6
Up-Regulation of OsBIHD1, a Rice Gene Encoding BELL Homeodomain Transcriptional Factor, in Disease Resistance Responses
journal, September 2005
- Luo, H.; Song, F.; Goodman, R. M.
- Plant Biology, Vol. 7, Issue 5
Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2
journal, June 2010
- Drigo, B.; Pijl, A. S.; Duyts, H.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 24
Promotion of Plant Growth by Bacterial ACC Deaminase
journal, October 2007
- Glick, Bernard R.; Todorovic, Biljana; Czarny, Jennifer
- Critical Reviews in Plant Sciences, Vol. 26, Issue 5-6
Isolation of tobacco ubiquitin‐conjugating enzyme cDNA in a yeast two‐hybrid system with tobacco ERF3 as bait and its characterization of specific interaction
journal, April 2003
- Koyama, Tomotsugu; Okada, Takashi; Kitajima, Sakihito
- Journal of Experimental Botany, Vol. 54, Issue 385
Activation of the Oryza sativa non-symbiotic haemoglobin-2 promoter by the cytokinin-regulated transcription factor, ARR1
journal, July 2004
- Ross, E. J. H.
- Journal of Experimental Botany, Vol. 55, Issue 403
Mastering ectomycorrhizal symbiosis: the impact of carbohydrates
journal, February 2008
- Nehls, U.
- Journal of Experimental Botany, Vol. 59, Issue 5
KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 1999
- Ogata, H.; Goto, S.; Sato, K.
- Nucleic Acids Research, Vol. 27, Issue 1
Plant cis-acting regulatory DNA elements (PLACE) database: 1999
journal, January 1999
- Higo, K.; Ugawa, Y.; Iwamoto, M.
- Nucleic Acids Research, Vol. 27, Issue 1
WoLF PSORT: protein localization predictor
journal, May 2007
- Horton, P.; Park, K. -J.; Obayashi, T.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Weights in the Balance: Jasmonic Acid and Salicylic Acid Signaling in Root-Biotroph Interactions
journal, July 2009
- Gutjahr, Caroline; Paszkowski, Uta
- Molecular Plant-Microbe Interactions®, Vol. 22, Issue 7
Combinatorial Interaction of Cis Elements Specifies the Expression of the Arabidopsis AtHsp90-1 Gene
journal, July 2002
- Haralampidis, Kosmas; Milioni, Dimitra; Rigas, Stamatis
- Plant Physiology, Vol. 129, Issue 3
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
Genome-Wide Identification of Potential Plant E2F Target Genes
journal, August 2005
- Vandepoele, Klaas; Vlieghe, Kobe; Florquin, Kobe
- Plant Physiology, Vol. 139, Issue 1
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
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
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
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
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
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
Absence of the endo-β-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato
journal, December 2007
- Flors, Víctor; Leyva, María de la O.; Vicedo, Begonya
- The Plant Journal, Vol. 52, Issue 6
Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure
journal, April 2005
- Gamper, Hannes; Hartwig, Ueli A.; Leuchtmann, Adrian
- New Phytologist, Vol. 167, Issue 2
The Laccaria genome: a symbiont blueprint decoded
journal, October 2008
- Martin, Francis; Selosse, Marc-André
- New Phytologist, Vol. 180, Issue 2
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate
journal, July 2010
- Beer, C.; Reichstein, M.; Tomelleri, E.
- Science, Vol. 329, Issue 5993
Molecular genetics of plant disease resistance
journal, May 1995
- Staskawicz, B.; Ausubel, F.; Baker, B.
- Science, Vol. 268, Issue 5211
Plant Immunity to Insect Herbivores
journal, June 2008
- Howe, Gregg A.; Jander, Georg
- Annual Review of Plant Biology, Vol. 59, Issue 1
Light-Regulated Transcription
journal, June 1995
- Terzaghi, William B.; Cashmore, Anthony R.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 46, Issue 1
A statistical method to incorporate biological knowledge for generating testable novel gene regulatory interactions from microarray experiments
journal, January 2007
- Larsen, Peter; Almasri, Eyad; Chen, Guanrao
- BMC Bioinformatics, Vol. 8, Issue 1
Rank-based edge reconstruction for scale-free genetic regulatory networks
journal, January 2008
- Chen, Guanrao; Larsen, Peter; Almasri, Eyad
- BMC Bioinformatics, Vol. 9, Issue 1
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
Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome
journal, January 2011
- Larsen, Peter E.; Sreedasyam, Avinash; Trivedi, Geetika
- BMC Systems Biology, Vol. 5, Issue 1
BowStrap v1.0: Assigning statistical significance to expressed genes using short-read transcriptome data
journal, June 2012
- Larsen, Peter E.; Collart, Frank R.
- BMC Research Notes, Vol. 5, Issue 1
TM4: A Free, Open-Source System for Microarray Data Management and Analysis
journal, February 2003
- Saeed, A. I.; Sharov, V.; White, J.
- BioTechniques, Vol. 34, Issue 2
Mycorrhizal Fungi
journal, January 1974
- Smith, S. E.
- CRC Critical Reviews in Microbiology, Vol. 3, Issue 3
Transcriptome responses to aluminum stress in roots of aspen (Populus tremula)
text, January 2010
- Nadine, Grisel,; Stefan, Zoller,; Marzanna, Künzli-Gontarczyk,
- ETH Zurich
Incorporating Network Topology Improves Prediction of Protein Interaction Networks from Transcriptomic Data
journal, July 2010
- Larsen, Peter E.; Collart, Frank; Dai, Yang
- International Journal of Knowledge Discovery in Bioinformatics, Vol. 1, Issue 3
Works referencing / citing this record:
Unearthing the roots of ectomycorrhizal symbioses
journal, October 2016
- Martin, Francis; Kohler, Annegret; Murat, Claude
- Nature Reviews Microbiology, Vol. 14, Issue 12
Dynamics of Aspen Roots Colonization by Pseudomonads Reveals Strain-Specific and Mycorrhizal-Specific Patterns of Biofilm Formation
journal, May 2018
- Noirot-Gros, Marie-Francoise; Shinde, Shalaka; Larsen, Peter E.
- Frontiers in Microbiology, Vol. 9
Data Integration in Poplar: ‘Omics Layers and Integration Strategies
journal, September 2019
- Weighill, Deborah; Tschaplinski, Timothy J.; Tuskan, Gerald A.
- Frontiers in Genetics, Vol. 10