Ethylene-Regulated Glutamate Dehydrogenase Fine-Tunes Metabolism during Anoxia-Reoxygenation.
Ethylene is an essential hormone in plants that is involved in low-oxygen and reoxygenation responses. As a key transcription factor in ethylene signaling, ETHYLENE INSENSITIVE3 (EIN3) activates targets that trigger various responses. However, most of these targets are still poorly characterized. Through analyses of our microarray data and the published Arabidopsis (Arabidopsis thaliana) EIN3 chromatin immunoprecipitation sequencing data set, we inferred the putative targets of EIN3 during anoxia-reoxygenation. Among them, GDH2, which encodes one subunit of glutamate dehydrogenase (GDH), was chosen for further studies for its role in tricarboxylic acid cycle replenishment. We demonstrated that both GDH1 and GDH2 are induced during anoxia and reoxygenation and that this induction is mediated via ethylene signaling. In addition, the results of enzymatic assays showed that the level of GDH during anoxia-reoxygenation decreased in the ethylene-insensitive mutants ein2-5 and ein3eil1 Global metabolite analysis indicated that the deamination activity of GDH might regenerate 2-oxoglutarate, which is a cosubstrate that facilitates the breakdown of alanine by alanine aminotransferase when reoxygenation occurs. Moreover, ineffective tricarboxylic acid cycle replenishment, disturbed carbohydrate metabolism, reduced phytosterol biosynthesis, and delayed energy regeneration were found in gdh1gdh2 and ethylene mutants during reoxygenation. Taken together, these data illustrate the essential role of EIN3-regulated GDH activity in metabolic adjustment during anoxia-reoxygenation.
Institute of Plant Biology, National Taiwan University, Taipei 115, Taiwan (K.-J.T., M.-C.S.); and.|Agricultural Biotechnology Research Center, Academia Sinica, Taipei 115, Taiwan (K.-J.T., C.-Y.L., C.-Y.T., M.-C.S.).
Kuen-Jin
0000-0002-8928-4331
KJ
Tsai
Institute of Plant Biology, National Taiwan University, Taipei 115, Taiwan (K.-J.T., M.-C.S.); and.|Agricultural Biotechnology Research Center, Academia Sinica, Taipei 115, Taiwan (K.-J.T., C.-Y.L., C.-Y.T., M.-C.S.).
Chih-Yu
0000-0002-3601-9032
CY
Lin
Institute of Plant Biology, National Taiwan University, Taipei 115, Taiwan (K.-J.T., M.-C.S.); and.|Agricultural Biotechnology Research Center, Academia Sinica, Taipei 115, Taiwan (K.-J.T., C.-Y.L., C.-Y.T., M.-C.S.).
Chen-Yun
0000-0002-5421-3402
CY
Ting
Institute of Plant Biology, National Taiwan University, Taipei 115, Taiwan (K.-J.T., M.-C.S.); and mcshih@gate.sinica.edu.tw.|Agricultural Biotechnology Research Center, Academia Sinica, Taipei 115, Taiwan (K.-J.T., C.-Y.L., C.-Y.T., M.-C.S.) mcshih@gate.sinica.edu.tw.
Ming-Che
0000-0002-7590-793X
MC
Shih
D000693:Anaerobiosis / Q000187:drug effects; D017360:Arabidopsis / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D050260:Carbohydrate Metabolism / Q000187:drug effects; D004268:DNA-Binding Proteins; D004734:Energy Metabolism / Q000187:drug effects; D005030:Ethylenes / Q000494:pharmacology*; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D005969:Glutamate Dehydrogenase / Q000378:metabolism*; D055442:Metabolome / Q000187:drug effects; D008954:Models, Biological; D009687:Nuclear Proteins / Q000378:metabolism; D010100:Oxygen / Q000378:metabolism*; D010641:Phenotype; D010840:Phytosterols / Q000096:biosynthesis; D055550:Protein Stability / Q000187:drug effects; D015398:Signal Transduction / Q000187:drug effects; D014157:Transcription Factors / Q000378:metabolism
D029681:Arabidopsis Proteins; D004268:DNA-Binding Proteins; C106987:EIN3 protein, Arabidopsis; D005030:Ethylenes; D009687:Nuclear Proteins; D010840:Phytosterols; D014157:Transcription Factors; C036216:ethylene; C000623006:GDH1 protein, Arabidopsis; C000623007:GDH2 protein, Arabidopsis; D005969:Glutamate Dehydrogenase; D010100:Oxygen
Plant J. 2007 Mar;49(6):1108-21
17319845
Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2992-7
12606727
Plant Cell. 2011 Nov;23(11):3944-60
22108404
Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):E203-12
24367078
Plant J. 2008 Dec;56(5):743-55
18665916
Nucleic Acids Res. 2010 Jul;38(Web Server issue):W64-70
20435677
Plant Physiol. 1989 Aug;90(4):1622-9
16666973
Elife. 2013 Jun 11;2:e00675
23795294
Ann Bot. 2009 Jan;103(2):197-209
19001425
Nature. 2009 Aug 20;460(7258):1026-30
19693083
Plant Physiol. 2016 Jan;170(1):43-56
26553649
J Exp Bot. 2012 Jul;63(12):4389-402
22585748
New Phytol. 2011 Apr;190(2):299-310
21108648
Mol Plant. 2011 Jul;4(4):626-34
21690206
Plant J. 2001 Sep;27(6):551-60
11576438
Plant Cell Physiol. 2009 Oct;50(10):1761-73
19690000
Nat Protoc. 2008;3(6):1101-8
18546601
Science. 2013 Aug 2;341(6145):508-13
23908229
J Exp Bot. 2008;59(9):2325-35
18508812
Proc Natl Acad Sci U S A. 2009 Nov 3;106(44):18843-8
19843695
Plant Physiol. 1992 Aug;99(4):1520-5
16669068
Plant Physiol. 2005 Mar;137(3):1115-29
15734912
Curr Opin Plant Biol. 2013 Oct;16(5):647-53
23830867
PLoS Genet. 2015 Mar 30;11(3):e1005143
25822663
J Exp Bot. 2015 Jun;66(11):3381-9
25878356
Plant Physiol. 2006 Jun;141(2):776-92
16603661
Science. 1999 Jun 25;284(5423):2148-52
10381874
Plant Biol (Stuttg). 2013 May;15(3):426-35
23574304
Curr Opin Plant Biol. 2013 Oct;16(5):554-60
24012247
Plant Physiol. 1991 Feb;95(2):509-16
16668014
New Phytol. 2012 Jun;194(4):895-909
22404712
Plant Signal Behav. 2008 Feb;3(2):133-4
19704733
Plant Physiol. 2010 Jun;153(2):757-72
20357136
Plant Physiol. 2010 Mar;152(3):1501-13
20089769
PLoS Genet. 2014 Oct 16;10(10):e1004664
25330213
Planta. 2004 Jun;219(2):286-97
14991406
Biophys J. 2010 Oct 6;99(7):2097-106
20923643
Plant J. 2003 Jan;33(2):341-52
12535347
Plant Physiol. 2012 Dec;160(4):1698-709
23093359
Plant Cell Physiol. 2008 Jan;49(1):92-102
18077464
Plant Physiol. 2011 May;156(1):202-12
21398256
Trends Plant Sci. 2004 Mar;9(3):110-5
15003233
Ann Bot. 2005 Sep;96(4):647-60
16081496
Nature. 2006 Aug 10;442(7103):705-8
16900200
Plant J. 2007 Mar;49(5):810-28
17257168
Plant Cell Environ. 2014 Oct;37(10):2366-80
24450922
FEBS Lett. 2008 Oct 29;582(25-26):3687-92
18848546
Plant Cell. 2012 Oct;24(10 ):4044-65
23054470
Plant Physiol. 2001 Jun;126(2):742-9
11402202
Plant Physiol. 2009 Sep;151(1):306-22
19571305
Proc Natl Acad Sci U S A. 1996 May 14;93(10):4718-23
8643469
Plant Cell. 2012 Jun;24(6):2578-95
22706288
Plant Physiol. 2010 Mar;152(3):1484-500
20097791
Plant Cell Physiol. 1997 Dec;38(12):1354-8
9522467
Plant Physiol. 1992 Mar;98(3):1190-5
16668745
J Exp Bot. 2008;59(3):667-80
18296429
Proc Natl Acad Sci U S A. 2014 Feb 11;111(6):2373-8
24469793
FASEB J. 2008 Nov;22(11):3980-91
18676403
Plant Cell Environ. 2014 Oct;37(10):2391-405
24506560
Plant Cell. 2006 Oct;18(10):2767-81
17041150
Plant Physiol. 1993 Nov;103(3):783-791
12231979