title: A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis.
abstract: Plants require daily coordinated regulation of energy metabolism for optimal growth and survival and therefore need to integrate cellular responses with both mitochondrial and plastid retrograde signaling. Using a forward genetic screen to characterize regulators of alternative oxidase1a (rao) mutants, we identified RAO2/Arabidopsis NAC domain-containing protein17 (ANAC017) as a direct positive regulator of AOX1a. RAO2/ANAC017 is targeted to connections and junctions in the endoplasmic reticulum (ER) and F-actin via a C-terminal transmembrane (TM) domain. A consensus rhomboid protease cleavage site is present in ANAC017 just prior to the predicted TM domain. Furthermore, addition of the rhomboid protease inhibitor N-p-Tosyl-l-Phe chloromethyl abolishes the induction of AOX1a upon antimycin A treatment. Simultaneous fluorescent tagging of ANAC017 with N-terminal red fluorescent protein (RFP) and C-terminal green fluorescent protein (GFP) revealed that the N-terminal RFP domain migrated into the nucleus, while the C-terminal GFP tag remained in the ER. Genome-wide analysis of the transcriptional network regulated by RAO2/ANAC017 under stress treatment revealed that RAO2/ANAC017 function was necessary for >85% of the changes observed as a primary response to cytosolic hydrogen peroxide (H2O2), but only ~33% of transcriptional changes observed in response to antimycin A treatment. Plants with mutated rao2/anac017 were more stress sensitive, whereas a gain-of-function mutation resulted in plants that had lower cellular levels of H2O2 under untreated conditions.
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia.
authors.forename: Sophia
authors.initials: S
authors.lastname: Ng
authors.forename: Aneta
authors.initials: A
authors.lastname: Ivanova
authors.forename: Owen
authors.initials: O
authors.lastname: Duncan
authors.forename: Simon R
authors.initials: SR
authors.lastname: Law
authors.forename: Olivier
authors.initials: O
authors.lastname: Van Aken
authors.forename: Inge
authors.initials: I
authors.lastname: De Clercq
authors.forename: Yan
authors.initials: Y
authors.lastname: Wang
authors.forename: Chris
authors.initials: C
authors.lastname: Carrie
authors.forename: Lin
authors.initials: L
authors.lastname: Xu
authors.forename: Beata
authors.initials: B
authors.lastname: Kmiec
authors.forename: Hayden
authors.initials: H
authors.lastname: Walker
authors.forename: Frank
authors.initials: F
authors.lastname: Van Breusegem
authors.forename: James
authors.initials: J
authors.lastname: Whelan
authors.forename: Estelle
authors.initials: E
authors.lastname: Giraud
mesh_terms: D017360:Arabidopsis / Q000166:cytology / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D001665:Binding Sites; D002467:Cell Nucleus / Q000378:metabolism; D004721:Endoplasmic Reticulum / Q000378:metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D017930:Genes, Reporter; D006861:Hydrogen Peroxide / Q000494:pharmacology; D008928:Mitochondria / Q000378:metabolism; D024101:Mitochondrial Proteins / Q000235:genetics / Q000378:metabolism; D009154:Mutation; D020411:Oligonucleotide Array Sequence Analysis; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D010641:Phenotype; D010802:Phylogeny; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D017434:Protein Structure, Tertiary; D011993:Recombinant Fusion Proteins; D036226:Seedlings / Q000166:cytology / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D015398:Signal Transduction; D013312:Stress, Physiological; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D059467:Transcriptome; D000099188:Alternative Oxidase
chemical_list: D029681:Arabidopsis Proteins; D006861:Hydrogen Peroxide; D024101:Mitochondrial Proteins; D010088:Oxidoreductases; D010940:Plant Proteins; D011993:Recombinant Fusion Proteins; D014157:Transcription Factors; D000099188:Alternative Oxidase; C000597111:ANAC017 protein, Arabidopsis
references.citation: Plant Physiol. 2013 May;162(1):254-71
references.pmid: 23509177
references.citation: Plant Physiol. 2008 Aug;147(4):1858-73
references.pmid: 18567827
references.citation: Mol Cell. 2004 Apr 9;14(1):1-15
references.pmid: 15068799
references.citation: Int J Mol Sci. 2013 Apr 15;14(4):8188-212
references.pmid: 23591838
references.citation: Plant Signal Behav. 2010 Jun;5(6):695-7
references.pmid: 20404498
references.citation: Biochem J. 2009 Jan 1;417(1):1-13
references.pmid: 19061483
references.citation: Proc Natl Acad Sci U S A. 2007 Jan 9;104(2):672-7
references.pmid: 17197417
references.citation: Adv Bioinformatics. 2008;2008:420747
references.pmid: 19956698
references.citation: Plant Physiol. 2008 Feb;146(2):748-61
references.pmid: 18055584
references.citation: J Biol Chem. 2012 Apr 6;287(15):11717-29
references.pmid: 22334687
references.citation: Plant Cell Physiol. 2013 Jun;54(6):971-81
references.pmid: 23539244
references.citation: Trends Cell Biol. 2007 Oct;17(10):511-7
references.pmid: 17851078
references.citation: Cell Res. 2008 Jul;18(7):756-67
references.pmid: 18427573
references.citation: Mol Cell. 2009 Dec 25;36(6):1048-59
references.pmid: 20064469
references.citation: Plant J. 2007 Sep;51(6):1126-36
references.pmid: 17666025
references.citation: Cell. 2001 Oct 19;107(2):173-82
references.pmid: 11672525
references.citation: Biochim Biophys Acta. 2005 Aug 15;1709(1):45-57
references.pmid: 16002040
references.citation: Bioinformatics. 2007 Nov 1;23(21):2947-8
references.pmid: 17846036
references.citation: Plant Mol Biol. 2005 May;58(2):159-75
references.pmid: 16027972
references.citation: AoB Plants. 2012;2012:pls014
references.pmid: 22708052
references.citation: Plant Physiol. 2009 Jul;150(3):1286-96
references.pmid: 19482916
references.citation: Annu Rev Plant Biol. 2013;64:477-99
references.pmid: 23330794
references.citation: Annu Rev Plant Biol. 2011;62:79-104
references.pmid: 21332361
references.citation: Mitochondrion. 2007 May;7(3):177-94
references.pmid: 17320492
references.citation: Genomics. 2010 Jan;95(1):56-65
references.pmid: 19766710
references.citation: J Biol Chem. 2013 Feb 1;288(5):3449-59
references.pmid: 23229550
references.citation: FEBS J. 2013 Apr;280(7):1579-603
references.pmid: 23432912
references.citation: Biochim Biophys Acta. 2012 Feb;1819(2):86-96
references.pmid: 21867785
references.citation: Plant Mol Biol. 2005 Apr;57(6):871-88
references.pmid: 15952071
references.citation: Biochim Biophys Acta. 2006 May-Jun;1763(5-6):450-62
references.pmid: 16624426
references.citation: Curr Opin Plant Biol. 2000 Oct;3(5):423-34
references.pmid: 11019812
references.citation: Plant J. 2005 Dec;44(5):744-55
references.pmid: 16297067
references.citation: Nat Rev Genet. 2008 May;9(5):383-95
references.pmid: 18368053
references.citation: Cell Signal. 2011 Jan;23(1):35-45
references.pmid: 20727407
references.citation: Cell. 1993 Sep 10;74(5):787-99
references.pmid: 7690685
references.citation: Cell Res. 2009 Nov;19(11):1279-90
references.pmid: 19752887
references.citation: Gene. 2010 Oct 1;465(1-2):30-44
references.pmid: 20600702
references.citation: Proc Natl Acad Sci U S A. 2012 Apr 3;109(14):5535-40
references.pmid: 22431637
references.citation: Trends Plant Sci. 2005 Feb;10(2):79-87
references.pmid: 15708345
references.citation: Cell. 2012 Jun 22;149(7):1525-35
references.pmid: 22726439
references.citation: Plant Cell. 2013 Apr;25(4):1416-29
references.pmid: 23624714
references.citation: Curr Opin Plant Biol. 2008 Dec;11(6):695-701
references.pmid: 19019722
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:703-734
references.pmid: 15012279
references.citation: Mol Biol Evol. 2011 Oct;28(10):2731-9
references.pmid: 21546353
references.citation: Nat Rev Genet. 2006 Jan;7(1):55-65
references.pmid: 16369572
references.citation: Trends Plant Sci. 2010 Jul;15(7):370-4
references.pmid: 20605736
references.citation: Plant Cell. 2004 Sep;16(9):2481-98
references.pmid: 15319476
references.citation: Plant J. 2004 Feb;37(3):379-90
references.pmid: 14731258
references.citation: Cell Motil Cytoskeleton. 2004 Oct;59(2):79-93
references.pmid: 15362112
references.citation: Annu Rev Plant Biol. 2002;53:247-73
references.pmid: 12221975
references.citation: Plant J. 2009 Mar;57(6):1128-39
references.pmid: 19036033
references.citation: Plant Mol Biol. 2007 Jan;63(1):97-108
references.pmid: 17120136
references.citation: Plant J. 2010 Apr;62(2):302-15
references.pmid: 20113439
references.citation: Biochem Soc Trans. 2010 Jun;38(3):789-95
references.pmid: 20491666
references.citation: Biochim Biophys Acta. 2012 Feb;1819(2):97-103
references.pmid: 22037288
references.citation: Nat Commun. 2012 Jun 26;3:926
references.pmid: 22735454
references.citation: Plant Cell. 2008 Nov;20(11):3107-21
references.pmid: 19017746
references.citation: Evolution. 1985 Jul;39(4):783-791
references.pmid: 28561359
references.citation: Plant J. 1998 Aug;15(3):441-7
references.pmid: 9750355
references.citation: J Exp Bot. 2002 Apr;53(369):659-67
references.pmid: 11886885
references.citation: Plant Cell. 2011 Nov;23(11):3992-4012
references.pmid: 22128124
references.citation: DNA Res. 2003 Dec 31;10(6):239-47
references.pmid: 15029955
references.citation: Plant Physiol. 2008 Jun;147(2):595-610
references.pmid: 18424626
references.citation: J Biol Chem. 2001 Jun 8;276(23):19937-44
references.pmid: 11259426
references.citation: Plant Physiol. 2006 Jun;141(2):436-45
references.pmid: 16603662
references.citation: Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):5280-5
references.pmid: 15781873
references.citation: Plant Physiol. 1989 Apr;89(4):1311-7
references.pmid: 16666702
references.citation: Plant Cell. 2012 Feb;24(2):482-506
references.pmid: 22345491
references.citation: Nat Commun. 2011 Sep 20;2:477
references.pmid: 21934661
references.citation: Plant Physiol. 2010 Mar;152(3):1674-92
references.pmid: 20107022
references.citation: J Cell Sci. 2010 May 1;123(Pt 9):1389-93
references.pmid: 20410371
references.citation: Plant Cell. 2012 Jun;24(6):2675-95
references.pmid: 22730406
references.citation: Proc Natl Acad Sci U S A. 2011 Apr 26;108(17):7247-52
references.pmid: 21482766
references.citation: Trends Plant Sci. 2010 Aug;15(8):427-35
references.pmid: 20580596
references.citation: Mol Plant. 2009 Nov;2(6):1310-24
references.pmid: 19995732
references.citation: Sci Rep. 2011;1:29
references.pmid: 22355548
references.citation: Biochem J. 2010 Apr 14;427(3):359-67
references.pmid: 20156199
references.citation: Comput Appl Biosci. 1992 Jun;8(3):275-82
references.pmid: 1633570
references.citation: Plant Cell. 2013 Sep;25(9):3472-90
references.pmid: 24045019