title: Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populus.
abstract: Salicylic acid (SA) has long been implicated in plant responses to oxidative stress. SA overproduction in Arabidopsis thaliana leads to dwarfism, making in planta assessment of SA effects difficult in this model system. We report that transgenic Populus tremula × alba expressing a bacterial SA synthase hyperaccumulated SA and SA conjugates without negative growth consequences. In the absence of stress, endogenously elevated SA elicited widespread metabolic and transcriptional changes that resembled those of wild-type plants exposed to oxidative stress-promoting heat treatments. Potential signaling and oxidative stress markers azelaic and gluconic acids as well as antioxidant chlorogenic acids were strongly coregulated with SA, while soluble sugars and other phenylpropanoids were inversely correlated. Photosynthetic responses to heat were attenuated in SA-overproducing plants. Network analysis identified potential drivers of SA-mediated transcriptome rewiring, including receptor-like kinases and WRKY transcription factors. Orthologs of Arabidopsis SA signaling components NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES1 and thioredoxins were not represented. However, all members of the expanded Populus nucleoredoxin-1 family exhibited increased expression and increased network connectivity in SA-overproducing Populus, suggesting a previously undescribed role in SA-mediated redox regulation. The SA response in Populus involved a reprogramming of carbon uptake and partitioning during stress that is compatible with constitutive chemical defense and sustained growth, contrasting with the SA response in Arabidopsis, which is transient and compromises growth if sustained.
authors.affiliation: Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA.
authors.forename: Liang-Jiao
authors.initials: LJ
authors.lastname: Xue
authors.forename: Wenbing
authors.initials: W
authors.lastname: Guo
authors.forename: Yinan
authors.initials: Y
authors.lastname: Yuan
authors.forename: Edward O
authors.initials: EO
authors.lastname: Anino
authors.forename: Batbayar
authors.initials: B
authors.lastname: Nyamdari
authors.forename: Mark C
authors.initials: MC
authors.lastname: Wilson
authors.forename: Christopher J
authors.initials: CJ
authors.lastname: Frost
authors.forename: Han-Yi
authors.initials: HY
authors.lastname: Chen
authors.forename: Benjamin A
authors.initials: BA
authors.lastname: Babst
authors.forename: Scott A
authors.initials: SA
authors.lastname: Harding
authors.forename: Chung-Jui
authors.initials: CJ
authors.lastname: Tsai
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental; D018506:Gene Expression Regulation, Plant; D063990:Gene Ontology; D053263:Gene Regulatory Networks; D006358:Hot Temperature; D008190:Lyases / Q000235:genetics / Q000378:metabolism; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism; D020411:Oligonucleotide Array Sequence Analysis; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D010788:Photosynthesis; D018515:Plant Leaves / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D032107:Populus / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism*; D020133:Reverse Transcriptase Polymerase Chain Reaction; D020156:Salicylic Acid / Q000378:metabolism*; D015398:Signal Transduction / Q000235:genetics; D059467:Transcriptome
chemical_list: D001426:Bacterial Proteins; D009687:Nuclear Proteins; D010940:Plant Proteins; D010088:Oxidoreductases; C105231:nucleoredoxin; D008190:Lyases; C022620:salicylate synthetase; D020156:Salicylic Acid
references.citation: Plant Cell Environ. 2011 Mar;34(3):434-43
references.pmid: 21062318
references.citation: Plant Physiol. 1999 Sep;121(1):147-52
references.pmid: 10482669
references.citation: Proc Natl Acad Sci U S A. 1996 May 14;93(10):5099-104
references.pmid: 8643534
references.citation: Bioinformatics. 2011 Feb 1;27(3):431-2
references.pmid: 21149340
references.citation: J Chem Ecol. 2010 Mar;36(3):286-97
references.pmid: 20177744
references.citation: Curr Opin Plant Biol. 2007 Oct;10(5):466-72
references.pmid: 17904410
references.citation: Plant Physiol. 2006 Jun;141(2):391-6
references.pmid: 16760493
references.citation: Photosynth Res. 2008 Oct-Dec;98(1-3):541-50
references.pmid: 18649006
references.citation: Plant J. 2004 Jul;39(2):147-60
references.pmid: 15225281
references.citation: Proc Natl Acad Sci U S A. 2011 Jul 26;108(30):12521-6
references.pmid: 21746919
references.citation: Philos Trans R Soc Lond B Biol Sci. 2012 Sep 19;367(1602):2619-39
references.pmid: 22889912
references.citation: Proc Natl Acad Sci U S A. 2009 Dec 22;106(51):22020-5
references.pmid: 19996170
references.citation: Mol Plant. 2009 Mar;2(2):308-22
references.pmid: 19825616
references.citation: Plant Physiol. 1999 Oct;121(2):489-96
references.pmid: 10517840
references.citation: Anal Chem. 2009 Dec 15;81(24):10038-48
references.pmid: 19928838
references.citation: New Phytol. 2011 Feb;189(3):678-687
references.pmid: 21087262
references.citation: Tree Physiol. 2010 Jan;30(1):32-44
references.pmid: 19864261
references.citation: Plant J. 1993 Oct;4(4):593-600
references.pmid: 8252063
references.citation: Plant Cell Environ. 2011 Sep;34(9):1488-506
references.pmid: 21554326
references.citation: Biotechniques. 2006 Dec;41(6):685-6
references.pmid: 17191609
references.citation: Cell. 1997 Jan 10;88(1):57-63
references.pmid: 9019406
references.citation: Annu Rev Phytopathol. 2009;47:177-206
references.pmid: 19400653
references.citation: Mol Plant Microbe Interact. 2008 May;21(5):507-17
references.pmid: 18393610
references.citation: Bioinformatics. 2006 Jul 1;22(13):1600-7
references.pmid: 16606683
references.citation: Plant Cell. 1995 Sep;7(9):1357-68
references.pmid: 8589621
references.citation: PLoS One. 2012;7(8):e44467
references.pmid: 22952983
references.citation: Curr Opin Plant Biol. 2001 Aug;4(4):309-14
references.pmid: 11418340
references.citation: Plant Physiol. 2008 Jul;147(3):1279-87
references.pmid: 18451262
references.citation: Am J Bot. 2012 Sep;99(9):e357-61
references.pmid: 22933359
references.citation: Plant J. 1999 May;18(3):321-7
references.pmid: 10377997
references.citation: Plant Physiol. 2004 Dec;136(4):4159-68
references.pmid: 15557093
references.citation: Plant Physiol. 2000 Jun;123(2):487-96
references.pmid: 10859179
references.citation: J Agric Food Chem. 2000 Nov;48(11):5512-6
references.pmid: 11087511
references.citation: Plant Cell. 1999 Aug;11(8):1393-404
references.pmid: 10449575
references.citation: Methods Mol Biol. 2006;344:143-51
references.pmid: 17033059
references.citation: J Exp Bot. 2006;57(8):1795-807
references.pmid: 16698814
references.citation: Ann Bot. 2006 Jul;98(1):33-40
references.pmid: 16675605
references.citation: BMC Plant Biol. 2009 Dec 29;9:151
references.pmid: 20040108
references.citation: J Chromatogr A. 2007 Jul 20;1157(1-2):414-21
references.pmid: 17543315
references.citation: Science. 1994 Nov 18;266(5188):1247-50
references.pmid: 17810266
references.citation: Phytochemistry. 2011 Sep;72(13):1497-509
references.pmid: 21376356
references.citation: Cell. 2006 Sep 8;126(5):969-80
references.pmid: 16959575
references.citation: Phytochemistry. 2007 Aug;68(15):2043-52
references.pmid: 17599371
references.citation: Plant Physiol. 2012 Sep;160(1):365-78
references.pmid: 22822212
references.citation: Plant Cell Physiol. 2001 Dec;42(12):1383-8
references.pmid: 11773531
references.citation: Plant Physiol. 2003 May;132(1):196-205
references.pmid: 12746525
references.citation: Cell Prolif. 2006 Apr;39(2):147-55
references.pmid: 16542349
references.citation: Plant Physiol. 2004 Oct;136(2):3364-75
references.pmid: 15448196
references.citation: Plant Physiol. 2010 Nov;154(3):1067-78
references.pmid: 20833726
references.citation: Bioinformatics. 2010 Apr 1;26(7):976-8
references.pmid: 20179076
references.citation: Curr Opin Plant Biol. 2003 Aug;6(4):339-42
references.pmid: 12873528
references.citation: J Bacteriol. 2003 Sep;185(18):5648-53
references.pmid: 12949119
references.citation: Plant Cell Physiol. 2012 Feb;53(2):e1
references.pmid: 22123792
references.citation: Nat Genet. 2005 Apr;37(4):382-90
references.pmid: 15778709
references.citation: Plant J. 1999 Mar;17(6):603-14
references.pmid: 10230060
references.citation: Science. 1999 Oct 15;286(5439):509-12
references.pmid: 10521342
references.citation: Nat Biotechnol. 2004 Jun;22(6):746-54
references.pmid: 15107863
references.citation: Z Naturforsch C J Biosci. 2004 Sep-Oct;59(9-10):684-92
references.pmid: 15540602
references.citation: Environ Pollut. 2011 Jan;159(1):45-54
references.pmid: 20980086
references.citation: Curr Opin Biotechnol. 2010 Oct;21(5):599-603
references.pmid: 20573499
references.citation: Bioinformatics. 2004 Sep 22;20(14):2242-50
references.pmid: 15130938
references.citation: Bioinformatics. 2011 Jan 15;27(2):225-31
references.pmid: 21098430
references.citation: Nat Biotechnol. 2000 Jul;18(7):779-83
references.pmid: 10888849
references.citation: Cell Rep. 2012 Jun 28;1(6):639-47
references.pmid: 22813739
references.citation: BMC Genomics. 2010 Nov 12;11:630
references.pmid: 21073700
references.citation: Plant Cell. 2005 Jul;17(7):1866-75
references.pmid: 15987996
references.citation: Science. 2009 Apr 3;324(5923):89-91
references.pmid: 19342588
references.citation: Plant Cell Environ. 2010 Oct;33(10):1742-55
references.pmid: 20525001
references.citation: Plant J. 2011 Sep;67(5):869-84
references.pmid: 21575090
references.citation: Plant Physiol. 2002 Feb;128(2):682-95
references.pmid: 11842171
references.citation: Nature. 2001 Nov 29;414(6863):562-5
references.pmid: 11734859
references.citation: Plant Cell Physiol. 2000 Sep;41(9):1038-44
references.pmid: 11100776
references.citation: Science. 1993 Aug 6;261(5122):754-6
references.pmid: 17757215
references.citation: Mol Plant Microbe Interact. 2009 Feb;22(2):190-200
references.pmid: 19132871
references.citation: Plant J. 2009 Nov;60(4):703-15
references.pmid: 19682285
references.citation: J Exp Bot. 2011 Jun;62(10):3321-38
references.pmid: 21357767
references.citation: Trends Plant Sci. 2010 Dec;15(12):693-700
references.pmid: 20961799
references.citation: Plant Cell. 2006 May;18(5):1310-26
references.pmid: 16603654
references.citation: BMC Bioinformatics. 2008 Dec 29;9:559
references.pmid: 19114008
references.citation: Plant J. 2004 May;38(3):432-47
references.pmid: 15086804
references.citation: Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2940-5
references.pmid: 10717008
references.citation: Science. 2008 Aug 15;321(5891):952-6
references.pmid: 18635760
references.citation: Nature. 2001 May 3;411(6833):41-2
references.pmid: 11333967
references.citation: Plant Biol (Stuttg). 2011 Jan;13(1):105-14
references.pmid: 21143731
references.citation: Plant Cell Environ. 2010 Jul;33(7):1220-33
references.pmid: 20199615
references.citation: Plant Physiol. 2004 Jan;134(1):460-9
references.pmid: 14730073
references.citation: New Phytol. 2006;172(1):47-62
references.pmid: 16945088
references.citation: Plant Physiol. 2009 May;150(1):12-26
references.pmid: 19321712
references.citation: New Phytol. 2005 Nov;168(2):351-64
references.pmid: 16219075
references.citation: Nucleic Acids Res. 2010 Jul;38(Web Server issue):W64-70
references.pmid: 20435677