title: Hormonal control of sulfate uptake and assimilation.
abstract: Plant hormones have a plethora of functions in control of plant development, stress response, and primary metabolism, including nutrient homeostasis. In the plant nutrition, the interplay of hormones with responses to nitrate and phosphate deficiency is well described, but relatively little is known about the interaction between phytohormones and regulation of sulfur metabolism. As for other nutrients, sulfate deficiency results in modulation of root architecture, where hormones are expected to play an important role. Accordingly, sulfate deficiency induces genes involved in metabolism of tryptophane and auxin. Also jasmonate biosynthesis is induced, pointing to the need of increase the defense capabilities of the plants when sulfur is limiting. However, hormones affect also sulfate uptake and assimilation. The pathway is coordinately induced by jasmonate and the key enzyme, adenosine 5'-phosphosulfate reductase, is additionally regulated by ethylene, abscisic acid, nitric oxid, and other phytohormones. Perhaps the most intriguing link between hormones and sulfate assimilation is the fact that the main regulator of the response to sulfate starvation, SULFATE LIMITATION1 (SLIM1) belongs to the family of ethylene related transcription factors. We will review the current knowledge of interplay between phytohormones and control of sulfur metabolism and discuss the main open questions.
authors.affiliation: Botanical Institute, Cluster of Excellence on Plant Sciences, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.
authors.forename: Anna
authors.initials: A
authors.lastname: Koprivova
authors.affiliation: Botanical Institute, Cluster of Excellence on Plant Sciences, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany. skopriva@uni-koeln.de.
authors.forename: Stanislav
authors.identifier: http://orcid.org/0000-0002-7416-6551
authors.initials: S
authors.lastname: Kopriva
mesh_terms: D010937:Plant Growth Regulators / Q000378:metabolism*; D015398:Signal Transduction; D013431:Sulfates / Q000378:metabolism*
chemical_list: D010937:Plant Growth Regulators; D013431:Sulfates
keywords: Cysteine; Glucosinolates; Glutathione; Phytohormones; Sulfate assimilation
references.citation: Plant Physiol. 2000 Mar;122(3):737-46
references.pmid: 10712537
references.citation: J Integr Plant Biol. 2015 Feb;57(2):186-97
references.pmid: 24798139
references.citation: Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):11102-7
references.pmid: 9380766
references.citation: Plant J. 2004 Jun;38(5):779-89
references.pmid: 15144379
references.citation: Plant Cell. 2010 Oct;22(10):3268-79
references.pmid: 20935247
references.citation: Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14819-24
references.pmid: 11114200
references.citation: Plant Cell Rep. 2010 Oct;29(10):1157-67
references.pmid: 20669021
references.citation: Plant Physiol Biochem. 2010 Dec;48(12):931-5
references.pmid: 20970349
references.citation: Plant J. 2014 Feb;77(4):604-15
references.pmid: 24330104
references.citation: PLoS One. 2007 Aug 08;2(8):e718
references.pmid: 17684564
references.citation: Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):15067-72
references.pmid: 19666544
references.citation: Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7623-7
references.pmid: 8755525
references.citation: Nitric Oxide. 2014 Sep 15;41:72-8
references.pmid: 24582856
references.citation: Elife. 2013 Jun 11;2:e00675
references.pmid: 23795294
references.citation: J Integr Plant Biol. 2014 Dec;56(12):1151-63
references.pmid: 24831283
references.citation: Plant Cell. 2000 Jan;12(1):97-110
references.pmid: 10634910
references.citation: PLoS One. 2012;7(10):e47797
references.pmid: 23112848
references.citation: Plant Physiol. 2003 Jan;131(1):298-308
references.pmid: 12529537
references.citation: Plant Mol Biol. 2005 Jul;58(4):497-513
references.pmid: 16021335
references.citation: Plant Physiol. 2014 Sep;166(1):349-69
references.pmid: 25049362
references.citation: Plant Physiol. 1984 Nov;76(3):579-83
references.pmid: 16663886
references.citation: Nature. 2005 Jan 6;433(7021):39-44
references.pmid: 15635403
references.citation: Plant J. 2009 Apr;58(2):299-317
references.pmid: 19170934
references.citation: Plant Physiol. 2004 Dec;136(4):4061-71
references.pmid: 15557090
references.citation: J Exp Bot. 2010 Jul;61(12):3395-405
references.pmid: 20566566
references.citation: Plant Cell. 2014 Oct;26(10):3984-98
references.pmid: 25326291
references.citation: J Exp Bot. 2010 Mar;61(3):889-900
references.pmid: 20018902
references.citation: Ann Bot. 2013 Dec;112(9):1655-65
references.pmid: 24136877
references.citation: Plant J. 2010 Apr 1;62(1):1-11
references.pmid: 20042022
references.citation: J Mol Biol. 2005 Apr 29;348(2):253-64
references.pmid: 15811366
references.citation: Plant Cell Environ. 2012 Feb;35(2):454-84
references.pmid: 21777251
references.citation: J Exp Bot. 2004 Aug;55(404):1799-808
references.pmid: 15234989
references.citation: Plant J. 2002 Sep;31(6):729-40
references.pmid: 12220264
references.citation: Plant Cell. 2006 Nov;18(11):3235-51
references.pmid: 17114350
references.citation: Plant J. 1998 May;14(3):337-44
references.pmid: 9628026
references.citation: Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2745-50
references.pmid: 11038608
references.citation: Plant Physiol. 2010 Mar;152(3):1335-45
references.pmid: 20053710
references.citation: New Phytol. 2010 Dec;188(4):977-84
references.pmid: 20831717
references.citation: J Exp Bot. 2014 Mar;65(5):1403-13
references.pmid: 24470466
references.citation: Annu Rev Plant Biol. 2002;53:247-73
references.pmid: 12221975
references.citation: J Exp Bot. 2004 Aug;55(404):1861-70
references.pmid: 15208339
references.citation: Plant Physiol. 2014 Dec;166(4):1803-20
references.pmid: 25352272
references.citation: Front Plant Sci. 2014 Oct 22;5:575
references.pmid: 25374579
references.citation: J Exp Bot. 2013 Dec;64(17):5281-96
references.pmid: 24014870
references.citation: J Biol Chem. 2001 Nov 2;276(44):40381-4
references.pmid: 11553608
references.citation: Trends Plant Sci. 2013 Jan;18(1):18-29
references.pmid: 23040678
references.citation: Plant Physiol. 2002 Nov;130(3):1406-13
references.pmid: 12428005
references.citation: PLoS One. 2012;7(6):e39425
references.pmid: 22724014
references.citation: Plant Physiol. 2004 Sep;136(1):2621-32
references.pmid: 15375207
references.citation: Plant Physiol. 2005 Jun;138(2):847-57
references.pmid: 15923327
references.citation: Plant Cell. 2011 Nov;23 (11):3992-4012
references.pmid: 22128124
references.citation: Plant Physiol. 2000 Jul;123(3):1163-71
references.pmid: 10889265
references.citation: Plant Cell. 2011 May;23 (5):1815-29
references.pmid: 21586684
references.citation: Cell. 1997 Jun 27;89(7):1133-44
references.pmid: 9215635
references.citation: Plant Physiol. 1988 Dec;88(4):1407-10
references.pmid: 16666474
references.citation: Photosynth Res. 2005 Dec;86(3):491-508
references.pmid: 16307302
references.citation: Plant Physiol. 2014 Nov;166(3):1593-608
references.pmid: 25245030
references.citation: Annu Rev Plant Biol. 2011;62:157-84
references.pmid: 21370978
references.citation: Plant J. 2004 Mar;37(5):770-7
references.pmid: 14871316
references.citation: Plant Cell. 2010 Feb;22(2):376-91
references.pmid: 20164444
references.citation: Plant Physiol. 2010 May;153(1):348-63
references.pmid: 20348214
references.citation: Plant J. 1999 Oct;20(1):37-44
references.pmid: 10571863
references.citation: Plant Physiol. 2014 Sep;166(1):442-50
references.pmid: 25049360
references.citation: Plant Cell. 2007 Jun;19(6):1851-65
references.pmid: 17586656
references.citation: Science. 2008 Aug 15;321(5891):952-6
references.pmid: 18635760
references.citation: Plant Physiol. 2008 Mar;146(3):1408-20
references.pmid: 18218969
references.citation: Biochem J. 2013 Apr 15;451(2):145-54
references.pmid: 23535167
references.citation: Planta. 2009 Jun;230(1):85-94
references.pmid: 19350269
references.citation: Genes Dev. 2001 Aug 1;15(15):1971-84
references.pmid: 11485991
references.citation: Plant Physiol. 2010 Mar;152(3):1357-72
references.pmid: 20044451
references.citation: Plant Physiol. 2014 Dec;166(4):2065-76
references.pmid: 25266633
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:249-279
references.pmid: 15012235
references.citation: Plant Cell. 2013 Aug;25(8):3117-32
references.pmid: 23943862
references.citation: Proc Natl Acad Sci U S A. 2013 Jun 4;110(23):9559-64
references.pmid: 23671085
references.citation: Front Plant Sci. 2015 Dec 01;6:1053
references.pmid: 26648954
references.citation: Plant J. 2007 Jun;50(5):886-901
references.pmid: 17461791
references.citation: Plant J. 2003 Feb;33(4):633-50
references.pmid: 12609038
references.citation: Planta. 2002 Apr;214(6):965-9
references.pmid: 11941474
references.citation: Nature. 2007 Oct 25;449(7165):1008-13
references.pmid: 17960234
references.citation: Trends Plant Sci. 2010 May;15(5):283-90
references.pmid: 20303821
references.citation: Nat Genet. 2007 Jul;39(7):896-900
references.pmid: 17589509
references.citation: Mol Plant. 2014 May;7(5):814-28
references.pmid: 24431192
references.citation: Plant J. 2004 Dec;40(6):893-908
references.pmid: 15584955
references.citation: Plant J. 2009 Apr;58(2):208-19
references.pmid: 19077168
references.citation: Plant Cell. 2001 Feb;13(2):351-67
references.pmid: 11226190
references.citation: Cell. 1994 Sep 23;78(6):931-6
references.pmid: 7923362
references.citation: Plant J. 2003 Feb;33(4):651-63
references.pmid: 12609039
references.citation: Plant Cell Physiol. 2002 Dec;43(12):1493-501
references.pmid: 12514246
references.citation: Plant Cell. 1995 Sep;7(9):1405-19
references.pmid: 8589625
references.citation: Plant J. 2005 May;42(3):305-14
references.pmid: 15842617
references.citation: Plant Physiol. 1991 Sep;97(1):253-8
references.pmid: 16668378
references.citation: Plant Physiol. 1978 Mar;61(3):342-7
references.pmid: 16660289
references.citation: Proc Natl Acad Sci U S A. 2007 Nov 13;104(46):18333-8
references.pmid: 17989228
references.citation: Planta. 2007 Apr;225(5):1233-44
references.pmid: 17039368
references.citation: Trends Plant Sci. 2006 Sep;11(9):440-8
references.pmid: 16899391
references.citation: Plant Mol Biol. 1999 Jul;40(4):729-36
references.pmid: 10480396
references.citation: Plant Cell. 1998 Sep;10(9):1539-50
references.pmid: 9724699
references.citation: Plant Cell Environ. 2010 Aug 1;33(8):1383-92
references.pmid: 20374532
references.citation: J Exp Bot. 2005 Jul;56(417):1887-96
references.pmid: 15911562
references.citation: Annu Rev Plant Biol. 2006;57:303-33
references.pmid: 16669764
references.citation: Front Plant Sci. 2014 Oct 29;5:589
references.pmid: 25400653
references.citation: Plant J. 2002 Feb;29(4):475-86
references.pmid: 11846880
references.citation: Plant Cell. 2009 Mar;21(3):910-27
references.pmid: 19304933