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 15 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. 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.
authors.affiliation: Argonne National Laboratory, Biosciences DivisionLemont, IL, USA; Department of Bioengineering, University of Illinois at ChicagoChicago IL, USA.
authors.forename: Peter E
authors.initials: PE
authors.lastname: Larsen
authors.affiliation: Department of Biological Sciences, University of Alabama in Huntsville Huntsville, AL, USA.
authors.forename: Avinash
authors.initials: A
authors.lastname: Sreedasyam
authors.affiliation: Department of Biological Sciences, University of Alabama in Huntsville Huntsville, AL, USA.
authors.forename: Geetika
authors.initials: G
authors.lastname: Trivedi
authors.affiliation: Argonne National Laboratory, Biosciences Division Lemont, IL, USA.
authors.forename: Shalaka
authors.initials: S
authors.lastname: Desai
authors.affiliation: Department of Bioengineering, University of Illinois at Chicago Chicago IL, USA.
authors.forename: Yang
authors.initials: Y
authors.lastname: Dai
authors.affiliation: Department of Biological Sciences, University of Alabama in Huntsville Huntsville, AL, USA.
authors.forename: Leland J
authors.initials: LJ
authors.lastname: Cseke
authors.affiliation: Argonne National Laboratory, Biosciences Division Lemont, IL, USA.
authors.forename: Frank R
authors.initials: FR
authors.lastname: Collart
keywords: Laccaria bicolor; Populus tremuloides; metabolomics; mycorrhizae; proteomics; system modeling; transcriptomics
references.citation: Plant Cell. 2006 Nov;18(11):2971-84
references.pmid: 17138697
references.citation: Annu Rev Plant Biol. 2008;59:41-66
references.pmid: 18031220
references.citation: J Mol Biol. 1993 Oct 20;233(4):580-96
references.pmid: 8411166
references.citation: Plant Physiol. 2009 Dec;151(4):1991-2005
references.pmid: 19854859
references.citation: Plant J. 2000 Dec;24(6):703-11
references.pmid: 11135105
references.citation: CRC Crit Rev Microbiol. 1974;3(3):275-313
references.pmid: 4604803
references.citation: EMBO J. 2002 Aug 15;21(16):4327-37
references.pmid: 12169635
references.citation: BMC Plant Biol. 2010 Aug 23;10:185
references.pmid: 20727216
references.citation: Mol Gen Genet. 1992 Jan;231(2):226-32
references.pmid: 1736093
references.citation: Plant Cell. 2003 Jun;15(6):1296-309
references.pmid: 12782724
references.citation: Gene. 1998 Nov 19;222(2):203-12
references.pmid: 9831654
references.citation: J Exp Bot. 2003 Apr;54(385):1175-81
references.pmid: 12654868
references.citation: Mol Plant Microbe Interact. 1995 Sep-Oct;8(5):781-3
references.pmid: 7579623
references.citation: BMC Res Notes. 2012 Jun 07;5:275
references.pmid: 22676709
references.citation: Mol Genet Genomics. 2009 Jul;282(1):1-15
references.pmid: 19488786
references.citation: BMC Plant Biol. 2009 Dec 29;9:151
references.pmid: 20040108
references.citation: Nat Methods. 2008 Jul;5(7):621-8
references.pmid: 18516045
references.citation: Mol Gen Genet. 1989 Jan;215(2):326-31
references.pmid: 2710102
references.citation: EMBO J. 1990 Jun;9(6):1717-26
references.pmid: 2347304
references.citation: Proc Natl Acad Sci U S A. 2010 Jun 15;107(24):10938-42
references.pmid: 20534474
references.citation: J Exp Bot. 2008;59(5):1097-108
references.pmid: 18272925
references.citation: Plant Cell Environ. 2013 May;36(5):909-19
references.pmid: 23145472
references.citation: Adv Exp Med Biol. 2011;705:271-94
references.pmid: 21618113
references.citation: Science. 1995 May 5;268(5211):661-7
references.pmid: 7732374
references.citation: Planta. 1992 Feb;186(3):409-17
references.pmid: 24186738
references.citation: Plant Mol Biol. 2002 Jun-Jul;49(3-4):373-85
references.pmid: 12036261
references.citation: Cell. 1990 Nov 30;63(5):1085-97
references.pmid: 2257625
references.citation: Plant Biol (Stuttg). 2005 Sep;7(5):459-68
references.pmid: 16163610
references.citation: FEBS J. 2011 Apr;278(7):1047-63
references.pmid: 21281447
references.citation: Plant Mol Biol. 1994 Jan;24(1):105-17
references.pmid: 8111010
references.citation: Trends Plant Sci. 2000 May;5(5):199-206
references.pmid: 10785665
references.citation: Plant J. 2007 Dec;52(6):1027-40
references.pmid: 17916112
references.citation: Plant Physiol. 2003 Sep;133(1):16-20
references.pmid: 12970469
references.citation: Biotechniques. 2003 Feb;34(2):374-8
references.pmid: 12613259
references.citation: BMC Bioinformatics. 2008 Jan 31;9:75
references.pmid: 18237422
references.citation: Plant J. 1994 Jun;5(6):815-26
references.pmid: 8054988
references.citation: Plant Cell. 2007 Jun;19(6):2077-89
references.pmid: 17601826
references.citation: Plant J. 2003 Mar;33(5):867-74
references.pmid: 12609028
references.citation: Science. 2006 Sep 15;313(5793):1596-604
references.pmid: 16973872
references.citation: Plant Cell. 2000 Mar;12(3):393-404
references.pmid: 10715325
references.citation: Curr Biol. 1998 Mar 26;8(7):R226-7
references.pmid: 9545207
references.citation: Microb Inform Exp. 2011 Jun 14;1(1):4
references.pmid: 22587810
references.citation: BMC Syst Biol. 2011 May 13;5:70
references.pmid: 21569493
references.citation: Int Rev Cytol. 1989;119:57-96
references.pmid: 2695485
references.citation: New Phytol. 2005 Aug;167(2):531-42
references.pmid: 15998404
references.citation: Curr Opin Plant Biol. 2007 Aug;10(4):393-8
references.pmid: 17658291
references.citation: Glycoconj J. 2004;20(7-8):449-60
references.pmid: 15316278
references.citation: Plant J. 2006 Jun;46(6):961-70
references.pmid: 16805730
references.citation: Plant Cell. 1997 Nov;9(11):1963-71
references.pmid: 9401121
references.citation: PLoS One. 2010 Jul 06;5(7):e9780
references.pmid: 20625404
references.citation: Photosynth Res. 1988 Apr;16(1-2):117-39
references.pmid: 24430995
references.citation: Plant Cell. 2003 Jan;15(1):63-78
references.pmid: 12509522
references.citation: BMC Bioinformatics. 2007 Aug 29;8:317
references.pmid: 17727721
references.citation: Trends Plant Sci. 2006 May;11(5):224-31
references.pmid: 16616581
references.citation: EMBO J. 1996 Oct 15;15(20):5690-700
references.pmid: 8896462
references.citation: Nucleic Acids Res. 2007 Jul;35(Web Server issue):W585-7
references.pmid: 17517783
references.citation: Nat Commun. 2010 Jul 27;1:48
references.pmid: 20975705
references.citation: Plant Physiol. 2002 Jul;129(3):1138-49
references.pmid: 12114568
references.citation: Plant Physiol. 2005 Sep;139(1):316-28
references.pmid: 16126853
references.citation: Biochim Biophys Acta. 2010 Feb;1800(2):190-201
references.pmid: 19647040
references.citation: Nat Genet. 2000 May;25(1):25-9
references.pmid: 10802651
references.citation: Nature. 2008 Sep 11;455(7210):195-200
references.pmid: 18690207
references.citation: Science. 2010 Aug 13;329(5993):834-8
references.pmid: 20603496
references.citation: Mol Plant Microbe Interact. 2009 Jul;22(7):763-72
references.pmid: 19522558
references.citation: Plant Physiol. 1997 May;114(1):15-27
references.pmid: 12223686
references.citation: Nucleic Acids Res. 1999 Jan 1;27(1):297-300
references.pmid: 9847208
references.citation: J Exp Bot. 2004 Aug;55(403):1721-31
references.pmid: 15258171
references.citation: Plant Cell. 2004 May;16(5):1077-90
references.pmid: 15100398
references.citation: Nucleic Acids Res. 1999 Jan 1;27(1):29-34
references.pmid: 9847135
references.citation: Trends Genet. 2000 Oct;16(10 ):449-55
references.pmid: 11050331
references.citation: Trends Plant Sci. 2012 May;17(5):260-70
references.pmid: 22498450
references.citation: Plant Physiol. 2004 Apr;134(4):1555-73
references.pmid: 15047898
references.citation: Plant Mol Biol. 2009 Mar;69(4):473-88
references.pmid: 19083153
references.citation: New Phytol. 2008;180(2):296-310
references.pmid: 19138220