title: Growth of Arabidopsis seedlings on high fungal doses of Piriformospora indica has little effect on plant performance, stress, and defense gene expression in spite of elevated jasmonic acid and jasmonic acid-isoleucine levels in the roots.
abstract: The endophytic fungus Piriformospora indica colonizes the roots of many plant species including Arabidopsis and promotes their performance, biomass, and seed production as well as resistance against biotic and abiotic stress. Imbalances in the symbiotic interaction such as uncontrolled fungal growth result in the loss of benefits for the plants and activation of defense responses against the microbe. We exposed Arabidopsis seedlings to a dense hyphal lawn of P. indica. The seedlings continue to grow, accumulate normal amounts of chlorophyll, and the photosynthetic parameters demonstrate that they perform well. In spite of high fungal doses around the roots, the fungal material inside the roots was not significantly higher when compared with roots that live in a beneficial symbiosis with P. indica. Fifteen defense- and stress-related genes including PR2, PR3, PAL2, and ERF1 are only moderately upregulated in the roots on the fungal lawn, and the seedlings did not accumulate H2O2/radical oxygen species. However, accumulation of anthocyanin in P. indica-exposed seedlings indicates stress symptoms. Furthermore, the jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) levels were increased in the roots, and consequently PDF1.2 and a newly characterized gene for a 2-oxoglurate and Fe2+ -dependent oxygenase were upregulated more than 7-fold on the dense fungal lawn, in a JAR1- and EIN3-dependent manner. We conclude that growth of A. thaliana seedlings on high fungal doses of P. indica has little effect on the overall performance of the plants although elevated JA and JA-Ile levels in the roots induce a mild stress or defense response.
authors.affiliation: Institute of Plant Physiology; Friedrich-Schiller-University Jena; Jena, Germany.
authors.forename: Khabat
authors.initials: K
authors.lastname: Vahabi
authors.affiliation: Institute of Plant Physiology; Friedrich-Schiller-University Jena; Jena, Germany.
authors.forename: Iris
authors.initials: I
authors.lastname: Camehl
authors.affiliation: Institute of Plant Physiology; Friedrich-Schiller-University Jena; Jena, Germany.
authors.forename: Irena
authors.initials: I
authors.lastname: Sherameti
authors.affiliation: Institute of Plant Physiology; Friedrich-Schiller-University Jena; Jena, Germany.
authors.forename: Ralf
authors.initials: R
authors.lastname: Oelmüller
mesh_terms: D000872:Anthocyanins / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics* / Q000276:immunology / Q000382:microbiology / Q000502:physiology*; D001487:Basidiomycota / Q000502:physiology*; D018533:Biomass; D002734:Chlorophyll / Q000378:metabolism; D003517:Cyclopentanes / Q000378:metabolism*; D004579:Electron Transport; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D005966:Glucuronidase / Q000378:metabolism; D006861:Hydrogen Peroxide / Q000378:metabolism; D007532:Isoleucine / Q000378:metabolism*; D009154:Mutation / Q000235:genetics; D025282:Mycelium / Q000254:growth & development; D054883:Oxylipins / Q000378:metabolism*; D010788:Photosynthesis; D018515:Plant Leaves / Q000378:metabolism / Q000382:microbiology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology; D018520:Plant Shoots / Q000254:growth & development; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D036226:Seedlings / Q000254:growth & development*; D013312:Stress, Physiological / Q000235:genetics; D015854:Up-Regulation / Q000235:genetics
chemical_list: D000872:Anthocyanins; D003517:Cyclopentanes; D054883:Oxylipins; D010940:Plant Proteins; D012333:RNA, Messenger; D007532:Isoleucine; D002734:Chlorophyll; C011006:jasmonic acid; D006861:Hydrogen Peroxide; D005966:Glucuronidase
keywords: H2O2; Piriformospora indica; defense; jasmonic acid; jasmonic acid-isoleucine; mutualistic plant/microbe interaction; stress response
references.citation: Mycorrhiza. 2005 Jul;15(5):373-9
references.pmid: 15875223
references.citation: Plant Cell. 2006 Apr;18(4):1052-66
references.pmid: 16517760
references.citation: FEBS Lett. 2008 Mar 19;582(6):967-76
references.pmid: 18307990
references.citation: Planta. 2008 May;227(6):1221-32
references.pmid: 18247047
references.citation: Plant Biol (Stuttg). 2010 Mar;12(2):292-301
references.pmid: 20398236
references.citation: Nucleic Acids Res. 2001 May 1;29(9):e45
references.pmid: 11328886
references.citation: Cell Res. 2010 May;20(5):539-52
references.pmid: 20354503
references.citation: Mol Plant Microbe Interact. 2009 Jul;22(7):763-72
references.pmid: 19522558
references.citation: Curr Opin Plant Biol. 2006 Aug;9(4):364-70
references.pmid: 16713732
references.citation: EMBO J. 2004 May 19;23(10):2071-82
references.pmid: 15116068
references.citation: Plant Cell. 1995 Jul;7(7):1085-1097
references.pmid: 12242399
references.citation: Plant Physiol. 2004 Nov;136(3):3824-37
references.pmid: 15489280
references.citation: Plant J. 2009 Apr;58(2):235-45
references.pmid: 19077166
references.citation: Plant Cell. 2004 Aug;16(8):2117-27
references.pmid: 15258265
references.citation: Nature. 2004 Feb 26;427(6977):858-61
references.pmid: 14985766
references.citation: Proc Natl Acad Sci U S A. 2010 Oct 19;107(42):18220-5
references.pmid: 20921422
references.citation: Mol Plant Microbe Interact. 2012 Sep;25(9):1186-97
references.pmid: 22852809
references.citation: PLoS Pathog. 2011 May;7(5):e1002051
references.pmid: 21625539
references.citation: Annu Rev Plant Biol. 2004;55:315-40
references.pmid: 15377223
references.citation: New Phytol. 2010 Jul;187(2):286-300
references.pmid: 20524992
references.citation: Mol Plant Microbe Interact. 2012 Jun;25(6):727-37
references.pmid: 22352718
references.citation: Curr Opin Plant Biol. 2009 Aug;12(4):500-7
references.pmid: 19576840
references.citation: Plant J. 2009 Apr;58(1):1-12
references.pmid: 19054359
references.citation: Plant Cell. 1998 Dec;10(12):2103-13
references.pmid: 9836748
references.citation: Nat Rev Microbiol. 2013 Apr;11(4):252-63
references.pmid: 23493145
references.citation: PLoS One. 2013;8(1):e53901
references.pmid: 23342034
references.citation: Genetics. 2006 Dec;174(4):1811-24
references.pmid: 17028338
references.citation: Plant J. 2008 May;54(3):428-39
references.pmid: 18248598
references.citation: Proc Natl Acad Sci U S A. 2005 May 31;102(22):8066-70
references.pmid: 15905328
references.citation: Plant Cell. 2003 Jan;15(1):165-78
references.pmid: 12509529
references.citation: Trends Plant Sci. 2012 Nov;17(11):633-7
references.pmid: 22818769
references.citation: Mol Plant Microbe Interact. 2008 Jun;21(6):799-807
references.pmid: 18624643
references.citation: Plant J. 2011 Sep;67(6):1029-41
references.pmid: 21615571
references.citation: J Integr Plant Biol. 2012 Jul;54(7):471-85
references.pmid: 22624950
references.citation: Front Plant Sci. 2013 Jul 11;4:228
references.pmid: 23874344
references.citation: Plant Signal Behav. 2011 Apr;6(4):553-7
references.pmid: 21422823
references.citation: Plant Physiol. 2011 Jun;156(2):726-40
references.pmid: 21474434
references.citation: Plant J. 2005 May;42(4):567-85
references.pmid: 15860015
references.citation: New Phytol. 2010 Oct;188(2):597-614
references.pmid: 20659300
references.citation: Annu Rev Microbiol. 2005;59:19-42
references.pmid: 16153162
references.citation: Plant Signal Behav. 2010 Aug;5(8):932-6
references.pmid: 20505369
references.citation: Plant Signal Behav. 2007 May;2(3):171-3
references.pmid: 19704747
references.citation: Plant J. 2009 Aug;59(3):461-74
references.pmid: 19392709
references.citation: Plant Cell. 1996 Dec;8(12):2309-23
references.pmid: 8989885
references.citation: Genes Dev. 1998 Dec 1;12(23):3703-14
references.pmid: 9851977
references.citation: Fungal Genet Biol. 2001 Jul;33(2):69-82
references.pmid: 11456460
references.citation: Planta. 2008 Sep;228(4):573-87
references.pmid: 18542996
references.citation: J Exp Bot. 2000 Apr;51(345):659-68
references.pmid: 10938857
references.citation: Plant Cell Rep. 2012 Jul;31(7):1269-81
references.pmid: 22466450
references.citation: New Phytol. 2010 Mar;185(4):1062-73
references.pmid: 20085621
references.citation: Plant J. 2006 Apr;46(1):34-53
references.pmid: 16553894
references.citation: PLoS Pathog. 2011 Oct;7(10):e1002290
references.pmid: 22022265
references.citation: Plant Physiol. 2010 Aug;153(4):1526-38
references.pmid: 20566705
references.citation: Plant Signal Behav. 2012 Dec;7(12):1584-8
references.pmid: 23073021
references.citation: Proc Natl Acad Sci U S A. 1985 Oct;82(20):6731-5
references.pmid: 16593613
references.citation: Mycologia. 2012 Jan-Feb;104(1):1-13
references.pmid: 21933929
references.citation: Plant Physiol. 2012 Dec;160(4):2173-88
references.pmid: 23073694
references.citation: Appl Environ Microbiol. 1999 Jun;65(6):2741-4
references.pmid: 10347070
references.citation: Science. 2009 May 8;324(5928):753-4
references.pmid: 19423817
references.citation: Proc Natl Acad Sci U S A. 1989 Dec;86(23):9284-8
references.pmid: 2594769
references.citation: Plant Physiol. 2004 Jul;135(3):1346-66
references.pmid: 15235117
references.citation: Mol Plant. 2013 May;6(3):872-86
references.pmid: 23118477
references.citation: Plant Cell. 2002 Jun;14(6):1405-15
references.pmid: 12084835
references.citation: Plant Physiol. 2008 Sep;148(1):436-54
references.pmid: 18650403
references.citation: Science. 2009 Jan 2;323(5910):95-101
references.pmid: 19095898
references.citation: Plant Physiol. 2004 Sep;136(1):2556-76
references.pmid: 15347784
references.citation: Plant J. 2009 Jul;59(2):193-206
references.pmid: 19392691
references.citation: J Chem Ecol. 2012 Jun;38(6):651-64
references.pmid: 22623151
references.citation: Plant Cell. 2006 Dec;18(12):3706-20
references.pmid: 17194769
references.citation: Curr Opin Plant Biol. 2006 Aug;9(4):358-63
references.pmid: 16713330
references.citation: Funct Integr Genomics. 2007 Jul;7(3):181-91
references.pmid: 17149585
references.citation: Mol Genet Genomics. 2007 Feb;277(2):115-37
references.pmid: 17061125
references.citation: Curr Opin Plant Biol. 2012 Dec;15(6):691-8
references.pmid: 23036821
references.citation: Science. 2003 Aug 15;301(5635):969-72
references.pmid: 12920300
references.citation: Plant J. 2002 Jan;29(1):23-32
references.pmid: 12060224