title: Roles of N-terminal fatty acid acylations in membrane compartment partitioning: Arabidopsis h-type thioredoxins as a case study.
abstract: N-terminal fatty acylations (N-myristoylation [MYR] and S-palmitoylation [PAL]) are crucial modifications affecting 2 to 4% of eukaryotic proteins. The role of these modifications is to target proteins to membranes. Predictive tools have revealed unexpected targets of these acylations in Arabidopsis thaliana and other plants. However, little is known about how N-terminal lipidation governs membrane compartmentalization of proteins in plants. We show here that h-type thioredoxins (h-TRXs) cluster in four evolutionary subgroups displaying strictly conserved N-terminal modifications. It was predicted that one subgroup undergoes only MYR and another undergoes both MYR and PAL. We used plant TRXs as a model protein family to explore the effect of MYR alone or MYR and PAL in the same family of proteins. We used a high-throughput biochemical strategy to assess MYR of specific TRXs. Moreover, various TRX-green fluorescent protein fusions revealed that MYR localized protein to the endomembrane system and that partitioning between this membrane compartment and the cytosol correlated with the catalytic efficiency of the N-myristoyltransferase acting at the N terminus of the TRXs. Generalization of these results was obtained using several randomly selected Arabidopsis proteins displaying a MYR site only. Finally, we demonstrated that a palmitoylatable Cys residue flanking the MYR site is crucial to localize proteins to micropatching zones of the plasma membrane.
authors.affiliation: Centre National de la Recherche Scientifique, Centre de Recherche de Gif, Institut des Sciences du Végétal, F-91198 Gif-sur-Yvette cedex, France.
authors.forename: José A
authors.initials: JA
authors.lastname: Traverso
authors.forename: Chiara
authors.initials: C
authors.lastname: Micalella
authors.forename: Aude
authors.initials: A
authors.lastname: Martinez
authors.forename: Spencer C
authors.initials: SC
authors.lastname: Brown
authors.forename: Béatrice
authors.initials: B
authors.lastname: Satiat-Jeunemaître
authors.forename: Thierry
authors.initials: T
authors.lastname: Meinnel
authors.forename: Carmela
authors.initials: C
authors.lastname: Giglione
mesh_terms: D000215:Acylation; D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D001665:Binding Sites; D002462:Cell Membrane / Q000235:genetics / Q000378:metabolism*; D003545:Cysteine / Q000235:genetics / Q000378:metabolism; D003600:Cytosol / Q000378:metabolism; D004721:Endoplasmic Reticulum / Q000378:metabolism; D004789:Enzyme Activation; D005227:Fatty Acids / Q000378:metabolism*; D036681:Fluorescence Recovery After Photobleaching; D049452:Green Fluorescent Proteins / Q000378:metabolism; D008563:Membrane Lipids / Q000378:metabolism*; D010802:Phylogeny; D021381:Protein Transport; D054480:Thioredoxin h / Q000235:genetics / Q000378:metabolism*
chemical_list: D005227:Fatty Acids; D008563:Membrane Lipids; D054480:Thioredoxin h; D049452:Green Fluorescent Proteins; D003545:Cysteine
references.citation: Mol Biol Cell. 2005 Sep;16(9):4061-72
references.pmid: 15975913
references.citation: Photosynth Res. 2006 Sep;89(2-3):179-92
references.pmid: 17031546
references.citation: Plant Physiol. 2012 Nov;160(3):1597-612
references.pmid: 22968831
references.citation: Biochim Biophys Acta. 2012 Dec;1823(12):2254-60
references.pmid: 23058975
references.citation: Anal Biochem. 2003 Nov 1;322(1):116-23
references.pmid: 14705787
references.citation: Plant Cell. 2011 Oct;23(10):3745-60
references.pmid: 22010036
references.citation: Biochemistry. 1998 Jul 14;37(28):10246-55
references.pmid: 9665732
references.citation: Proteomics. 2004 Jun;4(6):1626-32
references.pmid: 15174132
references.citation: PLoS One. 2008 Feb 20;3(2):e1620
references.pmid: 18286177
references.citation: Plant Cell. 2002 May;14(5):1077-92
references.pmid: 12034898
references.citation: Plant J. 2007 Sep;51(6):1126-36
references.pmid: 17666025
references.citation: Physiol Plant. 2008 Jul;133(3):611-22
references.pmid: 18384502
references.citation: J Biol Chem. 2003 Oct 31;278(44):43418-29
references.pmid: 12912986
references.citation: Neuron. 2004 Dec 16;44(6):987-96
references.pmid: 15603741
references.citation: Proc Natl Acad Sci U S A. 2004 Oct 5;101(40):14545-50
references.pmid: 15385674
references.citation: J Cell Sci. 2006 Dec 15;119(Pt 24):5087-97
references.pmid: 17158913
references.citation: Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):12805-10
references.pmid: 22689944
references.citation: J Chem Biol. 2010 Mar;3(1):19-35
references.pmid: 19898886
references.citation: Plant Signal Behav. 2008 Jul;3(7):501-2
references.pmid: 19704499
references.citation: Mol Plant. 2009 Mar;2(2):308-22
references.pmid: 19825616
references.citation: Science. 1987 Nov 27;238(4831):1275-8
references.pmid: 3685978
references.citation: Proc Natl Acad Sci U S A. 1985 Mar;82(6):1623-7
references.pmid: 2984663
references.citation: Mol Cancer Res. 2005 Aug;3(8):463-76
references.pmid: 16123142
references.citation: Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22050-4
references.pmid: 21131568
references.citation: J Mol Biol. 2002 Apr 5;317(4):541-57
references.pmid: 11955008
references.citation: Cell. 2010 Apr 30;141(3):458-71
references.pmid: 20416930
references.citation: Plant Cell. 2005 Sep;17(9):2554-63
references.pmid: 16100337
references.citation: Biochemistry. 1995 Mar 21;34(11):3813-22
references.pmid: 7893678
references.citation: Nat Chem Biol. 2009 Nov;5(11):835-41
references.pmid: 19749743
references.citation: J Biol Chem. 2001 Mar 30;276(13):10505-13
references.pmid: 11124252
references.citation: J Cell Biol. 2005 Feb 28;168(5):735-45
references.pmid: 15738266
references.citation: Trends Cell Biol. 1997 Jan;7(1):14-20
references.pmid: 17708893
references.citation: Proteomics. 2013 Jan;13(1):25-36
references.pmid: 23165749
references.citation: J Cell Sci. 2005 Feb 15;118(Pt 4):831-41
references.pmid: 15687105
references.citation: BMC Genomics. 2004 Jun 17;5(1):37
references.pmid: 15202951
references.citation: Biochemistry. 1994 Mar 15;33(10):3014-22
references.pmid: 8130214
references.citation: Science. 1996 Mar 15;271(5255):1519-26
references.pmid: 8599107
references.citation: Biochim Biophys Acta. 1998 Dec 8;1436(1-2):245-61
references.pmid: 9838145
references.citation: Proteomics. 2008 Feb;8(4):626-49
references.pmid: 18203265
references.citation: Nat Chem Biol. 2006 Nov;2(11):584-90
references.pmid: 17051234
references.citation: Plant J. 2000 Nov;24(4):429-35
references.pmid: 11115124
references.citation: Eur J Biochem. 2004 Feb;271(4):863-74
references.pmid: 14764103
references.citation: Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3900-5
references.pmid: 20133584
references.citation: Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W465-9
references.pmid: 18424797
references.citation: Cell Res. 2012 Jul;22(7):1155-68
references.pmid: 22547024
references.citation: Nat Rev Mol Cell Biol. 2007 Jan;8(1):74-84
references.pmid: 17183362
references.citation: Mol Cell Proteomics. 2007 Nov;6(11):1980-96
references.pmid: 17644812
references.citation: Biochim Biophys Acta. 1999 Nov 23;1441(2-3):162-72
references.pmid: 10570244
references.citation: Nature. 1985 Mar 28-Apr 3;314(6009):374-7
references.pmid: 3920530
references.citation: PLoS Biol. 2011 May;9(5):e1001074
references.pmid: 21655309
references.citation: Mol Plant Microbe Interact. 2012 Mar;25(3):379-92
references.pmid: 22046960
references.citation: Biochimie. 2011 Jan;93(1):18-31
references.pmid: 21056615
references.citation: Nat Cell Biol. 2003 May;5(5):373-6
references.pmid: 12724766
references.citation: Cell Mol Life Sci. 2004 Jun;61(12):1455-74
references.pmid: 15197470
references.citation: Mol Cell Biol. 1994 Jul;14(7):4722-30
references.pmid: 8007974
references.citation: Plant Cell. 2007 Sep;19(9):2804-21
references.pmid: 17827350
references.citation: Arch Biochem Biophys. 1988 Nov 1;266(2):496-507
references.pmid: 3190242
references.citation: Nat Struct Biol. 1998 Dec;5(12):1091-7
references.pmid: 9846880
references.citation: Annu Rev Genet. 2009;43:335-67
references.pmid: 19691428
references.citation: Plant Physiol. 2003 Jun;132(2):666-80
references.pmid: 12805596
references.citation: Proteomics. 2007 Oct;7(20):3788-99
references.pmid: 17828791
references.citation: Plant Cell. 2008 May;20(5):1346-62
references.pmid: 18502848
references.citation: Science. 2000 Dec 1;290(5497):1761-5
references.pmid: 11099414
references.citation: Proc Natl Acad Sci U S A. 1987 May;84(9):2708-12
references.pmid: 3106975
references.citation: Mol Cell Proteomics. 2012 Jun;11(6):M111.015131
references.pmid: 22223895
references.citation: Proteomics. 2008 Jul;8(14):2809-31
references.pmid: 18655050
references.citation: J Mol Biol. 2002 Apr 5;317(4):523-40
references.pmid: 11955007
references.citation: J Cell Sci. 2006 Sep 15;119(Pt 18):3743-53
references.pmid: 16926190
references.citation: Biochim Biophys Acta. 1999 Aug 12;1451(1):1-16
references.pmid: 10446384
references.citation: New Phytol. 2013 Feb;197(3):805-814
references.pmid: 23252521
references.citation: Plant Physiol. 2003 Aug;132(4):1840-8
references.pmid: 12913141
references.citation: Plant Physiol. 2002 Mar;128(3):1008-21
references.pmid: 11891256
references.citation: J Cell Biol. 1997 Jun 30;137(7):1525-35
references.pmid: 9199168
references.citation: Curr Opin Plant Biol. 2009 Dec;12(6):714-20
references.pmid: 19796984
references.citation: Science. 1997 Nov 7;278(5340):1132-5
references.pmid: 9353196
references.citation: Nat Struct Biol. 1996 Oct;3(10):842-8
references.pmid: 8836100
references.citation: J Biol Chem. 2005 May 13;280(19):18990-5
references.pmid: 15753093
references.citation: Plant Cell. 2009 May;21(5):1541-55
references.pmid: 19470590
references.citation: FEBS Lett. 2012 Mar 23;586(6):693-8
references.pmid: 22449965
references.citation: Mol Membr Biol. 1995 Oct-Dec;12(4):295-307
references.pmid: 8747274
references.citation: Cell Cycle. 2008 Dec;7(23):3709-19
references.pmid: 19029837
references.citation: Plant Cell. 2006 Nov;18(11):3182-200
references.pmid: 17138701
references.citation: Annu Rev Biochem. 1994;63:869-914
references.pmid: 7979256
references.citation: J Biol Chem. 1997 Nov 7;272(45):28680-9
references.pmid: 9353336
references.citation: Cell Signal. 1996 Sep;8(6):403-12
references.pmid: 8958442
references.citation: Science. 2010 Jan 1;327(5961):46-50
references.pmid: 20044567
references.citation: Mol Biol Cell. 1999 Nov;10(11):3771-86
references.pmid: 10564270
references.citation: Science. 1989 Feb 10;243(4892):796-800
references.pmid: 2644694
references.citation: Plant Cell. 2011 Apr;23(4):1191-3
references.pmid: 21531862
references.citation: Trends Cell Biol. 2005 Feb;15(2):84-91
references.pmid: 15695095
references.citation: Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3718-23
references.pmid: 10737809
references.citation: Biochemistry. 1993 Oct 5;32(39):10436-43
references.pmid: 8399188
references.citation: Front Biosci. 2008 May 01;13:6326-40
references.pmid: 18508663
references.citation: J Exp Bot. 2005 Jan;56(409):25-35
references.pmid: 15501910
references.citation: J Cell Sci. 2006 Apr 15;119(Pt 8):1494-503
references.pmid: 16537643
references.citation: J Cell Sci. 2002 Aug 1;115(Pt 15):3119-30
references.pmid: 12118067
references.citation: Plant J. 2010 Jan;61(2):211-22
references.pmid: 19832944
references.citation: EMBO J. 2000 Nov 1;19(21):5916-29
references.pmid: 11060042
references.citation: Mol Cell Proteomics. 2006 Dec;5(12):2336-49
references.pmid: 16963780
references.citation: Trends Biochem Sci. 1995 Jul;20(7):272-6
references.pmid: 7667880