title: The low energy signaling network.
abstract: Stress impacts negatively on plant growth and crop productivity, caicultural production worldwide. Throughout their life, plants are often confronted with multiple types of stress that affect overall cellular energy status and activate energy-saving responses. The resulting low energy syndrome (LES) includes transcriptional, translational, and metabolic reprogramming and is essential for stress adaptation. The conserved kinases sucrose-non-fermenting-1-related protein kinase-1 (SnRK1) and target of rapamycin (TOR) play central roles in the regulation of LES in response to stress conditions, affecting cellular processes and leading to growth arrest and metabolic reprogramming. We review the current understanding of how TOR and SnRK1 are involved in regulating the response of plants to low energy conditions. The central role in the regulation of cellular processes, the reprogramming of metabolism, and the phenotypic consequences of these two kinases will be discussed in light of current knowledge and potential future developments.
authors.affiliation: Bayer CropScience NV, Innovation Center Ghent, Belgium.
authors.forename: Filipa
authors.initials: F
authors.lastname: Tomé
authors.affiliation: Department of Ecogenomics and Systems Biology, University of Vienna Vienna, Austria.
authors.forename: Thomas
authors.initials: T
authors.lastname: Nägele
authors.affiliation: Instituto Gulbenkian de Ciência Oeiras, Portugal.
authors.forename: Mattia
authors.initials: M
authors.lastname: Adamo
authors.affiliation: Zentrum für Molekularbiologie der Pflanzen, Eberhard Karls Universität Tübingen Tübingen, Germany.
authors.forename: Abhroop
authors.initials: A
authors.lastname: Garg
authors.affiliation: Zentrum für Molekularbiologie der Pflanzen, Eberhard Karls Universität Tübingen Tübingen, Germany.
authors.forename: Carles
authors.initials: C
authors.lastname: Marco-Llorca
authors.affiliation: Department of Ecogenomics and Systems Biology, University of Vienna Vienna, Austria.
authors.forename: Ella
authors.initials: E
authors.lastname: Nukarinen
authors.affiliation: Julius-von-Sachs-Institut, Julius-Maximilians-Universität Würzburg Würzburg, Germany.
authors.forename: Lorenzo
authors.initials: L
authors.lastname: Pedrotti
authors.affiliation: Theoretical Biology and Bioinformatics, Department of Biology, Faculty of Science, Utrecht University Utrecht, Netherlands.
authors.forename: Alessia
authors.initials: A
authors.lastname: Peviani
authors.affiliation: Department of Ecogenomics and Systems Biology, University of Vienna Vienna, Austria.
authors.forename: Andrea
authors.initials: A
authors.lastname: Simeunovic
authors.affiliation: Universidad Politécnica de Madrid-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid Madrid, Spain.
authors.forename: Anna
authors.initials: A
authors.lastname: Tatkiewicz
authors.affiliation: Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University Utrecht, Netherlands.
authors.forename: Monika
authors.initials: M
authors.lastname: Tomar
authors.affiliation: Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University Utrecht, Netherlands.
authors.forename: Magdalena
authors.initials: M
authors.lastname: Gamm
keywords: SnRK1; T6P; TOR; bZIP; energy signaling; metabolism; stress
references.citation: Plant Cell Environ. 2012 Jan;35(1):1-21
references.pmid: 21477125
references.citation: EMBO Rep. 2007 Sep;8(9):864-70
references.pmid: 17721444
references.citation: Plant J. 2008 Mar;53(6):935-49
references.pmid: 18088315
references.citation: Curr Opin Chem Biol. 2009 Dec;13(5-6):532-8
references.pmid: 19837627
references.citation: Nature. 2007 Aug 23;448(7156):938-42
references.pmid: 17671505
references.citation: Biochem J. 2006 Jul 1;397(1):139-48
references.pmid: 16551270
references.citation: Prog Mol Biol Transl Sci. 2009;90:109-53
references.pmid: 20374740
references.citation: Mol Syst Biol. 2012 Mar 06;8:574
references.pmid: 22395476
references.citation: Plant Physiol. 2014 Feb;164(2):499-512
references.pmid: 24385567
references.citation: J Exp Bot. 2013 Nov;64(14):4361-74
references.pmid: 23963679
references.citation: Plant Physiol. 2006 Dec;142(4):1642-55
references.pmid: 17041027
references.citation: Plant Cell. 2009 Jun;21(6):1747-61
references.pmid: 19531597
references.citation: Trends Plant Sci. 2008 Apr;13(4):165-71
references.pmid: 18329321
references.citation: Curr Opin Plant Biol. 2003 Jun;6(3):247-56
references.pmid: 12753974
references.citation: Plant Cell. 2011 Jan;23(1):381-95
references.pmid: 21278122
references.citation: J Mol Cell Biol. 2011 Aug;3(4):206-20
references.pmid: 21138990
references.citation: Mol Plant. 2010 Mar;3(2):361-73
references.pmid: 20080816
references.citation: Plant Cell. 2008 Dec;20(12):3430-47
references.pmid: 19060111
references.citation: J Mol Evol. 2011 Oct;73(3-4):209-20
references.pmid: 22057117
references.citation: J Exp Bot. 2014 Mar;65(3):799-807
references.pmid: 24453229
references.citation: Proc Natl Acad Sci U S A. 2003 May 27;100(11):6849-54
references.pmid: 12748379
references.citation: Planta. 2012 Aug;236(2):355-69
references.pmid: 22367062
references.citation: Proc Natl Acad Sci U S A. 2004 Jul 6;101(27):10205-10
references.pmid: 15199185
references.citation: Trends Plant Sci. 2008 May;13(5):247-55
references.pmid: 18424222
references.citation: Plant Physiol. 2009 Jul;150(3):1356-67
references.pmid: 19403731
references.citation: Plant J. 2012 Jun;70(6):954-66
references.pmid: 22288575
references.citation: Nature. 2013 Apr 11;496(7444):181-6
references.pmid: 23542588
references.citation: Int J Biochem Cell Biol. 2006;38(9):1476-81
references.pmid: 16647875
references.citation: Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3730-4
references.pmid: 10725382
references.citation: J Biol Chem. 2010 Apr 16;285(16):12071-7
references.pmid: 20164192
references.citation: Nat Cell Biol. 2011 Feb;13(2):132-41
references.pmid: 21258367
references.citation: Plant J. 1999 Aug;19(4):433-9
references.pmid: 10504565
references.citation: Annu Rev Plant Biol. 2006;57:781-803
references.pmid: 16669782
references.citation: New Phytol. 2011 Aug;191(3):733-745
references.pmid: 21534971
references.citation: Glycobiology. 2003 Apr;13(4):17R-27R
references.pmid: 12626396
references.citation: Plant Physiol. 2013 Jul;162(3):1246-65
references.pmid: 23674104
references.citation: Mol Plant. 2013 Nov;6(6):1731-3
references.pmid: 23761348
references.citation: J Exp Bot. 2001 May;52(358):1063-70
references.pmid: 11432922
references.citation: Mol Syst Biol. 2012;8:606
references.pmid: 22929616
references.citation: Plant Physiol. 1995 Jul;108(3):1077-1082
references.pmid: 12228528
references.citation: Plant Physiol. 2012 Apr;158(4):1955-64
references.pmid: 22232383
references.citation: Plant Cell Physiol. 2009 Dec;50(12):2123-32
references.pmid: 19880399
references.citation: Plant J. 2007 Feb;49(3):463-91
references.pmid: 17217462
references.citation: EMBO J. 2013 Apr 17;32(8):1069-71
references.pmid: 23524852
references.citation: Plant J. 1998 Jul;15(2):253-63
references.pmid: 9721683
references.citation: Genes Dev. 2004 Aug 15;18(16):1926-45
references.pmid: 15314020
references.citation: Biochem J. 1997 Jul 1;325 ( Pt 1):101-9
references.pmid: 9245257
references.citation: Plant J. 2004 Mar;37(6):914-39
references.pmid: 14996223
references.citation: PLoS One. 2008 Aug 13;3(8):e2944
references.pmid: 18698409
references.citation: Cell Cycle. 2010 Mar 1;9(5):953-7
references.pmid: 20038818
references.citation: Plant J. 2005 Apr;42(2):218-35
references.pmid: 15807784
references.citation: J Biol Chem. 2005 Jul 8;280(27):25590-5
references.pmid: 15866872
references.citation: Plant J. 2010 Oct;64(1):1-13
references.pmid: 20659274
references.citation: Curr Opin Plant Biol. 2009 Apr;12(2):223-30
references.pmid: 19162531
references.citation: Science. 2013 May 10;340(6133):730-4
references.pmid: 23661758
references.citation: Plant Mol Biol. 1998 Jul;37(5):735-48
references.pmid: 9678569
references.citation: Annu Rev Plant Biol. 2008;59:417-41
references.pmid: 18257709
references.citation: Front Plant Sci. 2014 Apr 01;5:119
references.pmid: 24744765
references.citation: Mol Syst Biol. 2010 Sep 21;6:416
references.pmid: 20865009
references.citation: EMBO J. 2013 Apr 17;32(8):1087-102
references.pmid: 23524850
references.citation: Plant J. 2004 Jun;38(5):823-39
references.pmid: 15144383
references.citation: FEBS J. 2011 Nov;278(21):3978-90
references.pmid: 21883929
references.citation: Trends Plant Sci. 2007 May;12(5):185-8
references.pmid: 17412635
references.citation: Plant Mol Biol. 2009 Jan;69(1-2):107-19
references.pmid: 18841482
references.citation: J Exp Bot. 2004 Jan;55(395):225-36
references.pmid: 14673035
references.citation: Biochem Biophys Res Commun. 2005 Jan 28;326(4):844-50
references.pmid: 15607746
references.citation: Plant Cell. 2013 Oct;25(10):3871-84
references.pmid: 24179127
references.citation: Trends Plant Sci. 2007 Jan;12(1):20-8
references.pmid: 17166759
references.citation: Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6478-83
references.pmid: 17420480
references.citation: Mol Syst Biol. 2009;5:314
references.pmid: 19888209
references.citation: J Exp Bot. 2014 Jun;65(10):2703-14
references.pmid: 24218325
references.citation: Mol Biol Cell. 2004 Feb;15(2):946-56
references.pmid: 14595104
references.citation: Plant Physiol. 2013 Jul;162(3):1720-32
references.pmid: 23735508
references.citation: Plant Cell. 2012 Feb;24(2):463-81
references.pmid: 22307851
references.citation: Mol Syst Biol. 2013;9:650
references.pmid: 23511208
references.citation: J Exp Bot. 2013 Nov;64(14):4301-12
references.pmid: 23997203
references.citation: Front Plant Sci. 2013 Jul 24;4:272
references.pmid: 23898339
references.citation: Annu Rev Pharmacol Toxicol. 2012;52:381-400
references.pmid: 22017684
references.citation: J Exp Bot. 2008;59(3):667-80
references.pmid: 18296429
references.citation: Front Plant Sci. 2013 Aug 01;4:282
references.pmid: 23914195
references.citation: Plant Mol Biol. 2004 Nov;56(5):747-59
references.pmid: 15803412
references.citation: Gene. 2013 Jan 10;512(2):364-72
references.pmid: 23107762
references.citation: Plant Cell. 2004 Jul;16(7):1717-29
references.pmid: 15208401
references.citation: Biochem J. 2009 Apr 15;419(2):247-59
references.pmid: 19309312
references.citation: J Biol Chem. 2012 Jan 20;287(4):2836-42
references.pmid: 22134914
references.citation: Crit Rev Food Sci Nutr. 2012;52(5):373-81
references.pmid: 22369257
references.citation: Plant Cell Environ. 2015 Jan;38(1):35-49
references.pmid: 24738645
references.citation: Plant Physiol. 2003 Jun;132(2):666-80
references.pmid: 12805596
references.citation: Genes Dev. 2004 Oct 15;18(20):2431-6
references.pmid: 15489289
references.citation: Nature. 2006 Aug 31;442(7106):1058-61
references.pmid: 16900101
references.citation: Plant Cell. 2012 Dec;24(12):4850-74
references.pmid: 23275579
references.citation: Plant J. 1999 Jun;18(5):541-50
references.pmid: 10417704
references.citation: Annu Rev Biochem. 1998;67:821-55
references.pmid: 9759505
references.citation: Eur J Biochem. 1992 Nov 1;209(3):923-31
references.pmid: 1358611
references.citation: J Exp Bot. 2011 Jan;62(3):883-93
references.pmid: 20974737
references.citation: Plant Physiol. 2004 Aug;135(4):2330-47
references.pmid: 15310832
references.citation: Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6422-7
references.pmid: 11983923
references.citation: Front Plant Sci. 2012 Apr 05;3:66
references.pmid: 22645595
references.citation: Plant Physiol. 2011 Mar;155(3):1367-82
references.pmid: 21266656
references.citation: Plant Cell. 2005 Dec;17(12):3257-81
references.pmid: 16299223
references.citation: Annu Rev Plant Biol. 2006;57:675-709
references.pmid: 16669778
references.citation: Plant J. 2014 Aug;79(4):544-67
references.pmid: 24645920
references.citation: Plant Physiol. 2009 Apr;149(4):1860-71
references.pmid: 19193861
references.citation: Mol Plant. 2013 Mar;6(2):261-74
references.pmid: 23100484
references.citation: Plant Cell Environ. 2008 Oct;31(10):1399-409
references.pmid: 18643951
references.citation: Crit Rev Biochem Mol Biol. 2009 Jul-Aug;44(4):143-68
references.pmid: 19604130
references.citation: Plant J. 2011 Sep;67(5):869-84
references.pmid: 21575090
references.citation: Plant Cell Physiol. 2004 Mar;45(3):309-17
references.pmid: 15047879
references.citation: Plant Physiol. 2004 Jun;135(2):879-90
references.pmid: 15181209
references.citation: Plant J. 2013 Mar;73(6):897-909
references.pmid: 23173928
references.citation: Plant J. 2004 Sep;39(6):847-62
references.pmid: 15341628
references.citation: PLoS Biol. 2006 Oct;4(10):e312
references.pmid: 16968132
references.citation: BMC Plant Biol. 2007 Jun 01;7:26
references.pmid: 17543119
references.citation: Ann Bot. 2005 Sep;96(4):647-60
references.pmid: 16081496
references.citation: Mol Cell Proteomics. 2005 Oct;4(10):1614-25
references.pmid: 16030010
references.citation: Genome Biol. 2006;7(8):R76
references.pmid: 16916443
references.citation: Plant J. 2008 Dec;56(5):743-55
references.pmid: 18665916
references.citation: EMBO J. 1990 Aug;9(8):2439-46
references.pmid: 2369897
references.citation: Plant Physiol. 2006 Jun;141(2):663-73
references.pmid: 16632591
references.citation: Genes Dev. 2004 Oct 15;18(20):2491-505
references.pmid: 15466158
references.citation: Proc Natl Acad Sci U S A. 2009 Nov 3;106(44):18843-8
references.pmid: 19843695
references.citation: Plant Signal Behav. 2008 Oct;3(10):842-3
references.pmid: 19704517
references.citation: Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):5104-9
references.pmid: 21383174
references.citation: New Phytol. 2013 May;198(3):777-787
references.pmid: 23488986
references.citation: Front Plant Sci. 2014 May 16;5:199
references.pmid: 24904601
references.citation: Plant J. 2002 Apr;30(2):221-35
references.pmid: 12000458
references.citation: Mol Plant. 2010 Mar;3(2):300-13
references.pmid: 20080814
references.citation: Trends Plant Sci. 2012 Mar;17(3):129-38
references.pmid: 22280796
references.citation: Metabolites. 2012 Sep 06;2(3):553-66
references.pmid: 24957647
references.citation: Trends Plant Sci. 2002 Mar;7(3):106-11
references.pmid: 11906833
references.citation: Trends Plant Sci. 2008 Sep;13(9):474-82
references.pmid: 18701338
references.citation: Plant Cell. 2011 Jan;23(1):185-209
references.pmid: 21216945
references.citation: BMC Syst Biol. 2013 Mar 19;7:23
references.pmid: 23506153
references.citation: Nat Rev Mol Cell Biol. 2013 Mar;14(3):133-9
references.pmid: 23361334
references.citation: J Exp Bot. 2011 Mar;62(6):1715-29
references.pmid: 21239376
references.citation: Front Plant Sci. 2013 Jun 20;4:197
references.pmid: 23802004
references.citation: Curr Opin Plant Biol. 2012 Jun;15(3):301-7
references.pmid: 22305521
references.citation: Curr Opin Cell Biol. 2005 Apr;17(2):158-66
references.pmid: 15780592
references.citation: J Exp Bot. 2014 Mar;65(4):1051-68
references.pmid: 24420566
references.citation: J Exp Bot. 2004 Jan;55(394):35-42
references.pmid: 14645392
references.citation: Cell. 2004 Dec 29;119(7):969-79
references.pmid: 15620355
references.citation: J R Soc Interface. 2013 Dec 11;11(91):20130979
references.pmid: 24335560
references.citation: EMBO J. 2006 Jul 12;25(13):3133-43
references.pmid: 16810321
references.citation: Plant Methods. 2013 Jun 20;9(1):21
references.pmid: 23786766
references.citation: Nat Rev Mol Cell Biol. 2009 May;10(5):307-18
references.pmid: 19339977
references.citation: Plant Physiol. 2008 Apr;146(4):1834-61
references.pmid: 18305208
references.citation: Cell. 2006 Feb 10;124(3):471-84
references.pmid: 16469695
references.citation: Genes Dev. 2004 Feb 15;18(4):423-34
references.pmid: 15004009
references.citation: J Exp Bot. 2003 Jan;54(382):539-47
references.pmid: 12508065