Arabidopsis LIM proteins: a family of actin bundlers with distinct expression patterns and modes of regulation.
Recently, a number of two LIM-domain containing proteins (LIMs) have been reported to trigger the formation of actin bundles, a major higher-order cytoskeletal assembly. Here, we analyzed the six Arabidopsis thaliana LIM proteins. Promoter-β-glucuronidase reporter studies revealed that WLIM1, WLIM2a, and WLIM2b are widely expressed, whereas PLIM2a, PLIM2b, and PLIM2c are predominantly expressed in pollen. LIM-green fluorescent protein (GFP) fusions all decorated the actin cytoskeleton and increased actin bundle thickness in transgenic plants and in vitro, although with different affinities and efficiencies. Remarkably, the activities of WLIMs were calcium and pH independent, whereas those of PLIMs were inhibited by high pH and, in the case of PLIM2c, by high [Ca(2+)]. Domain analysis showed that the C-terminal domain is key for the responsiveness of PLIM2c to pH and calcium. Regulation of LIM by pH was further analyzed in vivo by tracking GFP-WLIM1 and GFP-PLIM2c during intracellular pH modifications. Cytoplasmic alkalinization specifically promoted release of GFP-PLIM2c but not GFP-WLIM1, from filamentous actin. Consistent with these data, GFP-PLIM2c decorated long actin bundles in the pollen tube shank, a region of relatively low pH. Together, our data support a prominent role of Arabidopsis LIM proteins in the regulation of actin cytoskeleton organization and dynamics in sporophytic tissues and pollen.
Papuga
Jessica
J
Centre de Recherche Public-Santé, L-1526 Luxembourg, Luxembourg.
Hoffmann
Céline
C
Dieterle
Monika
M
Moes
Danièle
D
Moreau
Flora
F
Tholl
Stéphane
S
Steinmetz
André
A
Thomas
Clément
C
D008841:Actin Cytoskeleton / Q000378:metabolism*; D000199:Actins / Q000378:metabolism*; D017360:Arabidopsis / Q000235:genetics* / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002118:Calcium / Q000378:metabolism; D002352:Carrier Proteins / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D006863:Hydrogen-Ion Concentration; D008840:Microfilament Proteins / Q000235:genetics / Q000378:metabolism*; D030821:Plants, Genetically Modified / Q000235:genetics / Q000378:metabolism; D053205:Pollen Tube / Q000254:growth & development
D000199:Actins; D029681:Arabidopsis Proteins; D002352:Carrier Proteins; D008840:Microfilament Proteins; C416644:PLIM1 protein, Arabidopsis; D002118:Calcium
Plant Cell. 2005 Aug;17(8):2296-313
15994911
Plant Physiol. 2007 Nov;145(3):747-62
17905860
Structure. 2004 Jun;12(6):999-1013
15274920
Plant Cell. 2008 Mar;20(3):614-34
18364468
Plant J. 2000 Dec;24(5):625-36
11123801
Plant Mol Biol. 2000 Jan;42(2):291-302
10794529
J Cell Sci. 1997 Jun;110 ( Pt 11):1269-78
9202387
Bioessays. 2001 Jan;23(1):86-94
11135313
Plant Cell. 2006 Sep;18(9):2182-93
16920777
Dev Dyn. 1999 Mar;214(3):229-38
10090149
Plant Cell. 1999 Jun;11(6):995-1006
10368172
Plant Cell. 2006 Sep;18(9):2194-206
16905656
Annu Rev Plant Biol. 2008;59:547-72
18444907
Curr Biol. 2006 Oct 10;16(19):1924-30
17027489
Science. 2003 Oct 31;302(5646):842-6
14593172
Plant Mol Biol. 1998 Jan;36(1):23-31
9484459
New Phytol. 2008;177(2):525-536
18028299
Plant Physiol. 2009 Jul;150(3):1322-34
19474213
J Cell Biol. 1997 Oct 6;139(1):157-68
9314536
Protoplasma. 2001;215(1-4):64-76
11732066
J Cell Sci. 1997 May;110 ( Pt 10):1187-98
9191043
Plant Cell. 2009 Dec;21(12):3868-84
20023198
Mol Gen Genet. 2000 Oct;264(3):257-67
11085265
Plant Physiol. 2008 Aug;147(4):1619-36
18480376
Plant Physiol. 2004 Dec;136(4):3979-89
15557101
Plant Cell. 2002 Sep;14(9):2175-90
12215514
Plant Cell. 2007 Oct;19(10):3111-26
17933902
Philos Trans R Soc Lond B Biol Sci. 2002 Jun 29;357(1422):791-8
12079674
Dev Biol. 1996 Feb 25;174(1):160-73
8626016
J Plant Res. 2007 Jan;120(1):31-43
17252175
Plant Mol Biol. 2003 Jul;52(4):715-27
13677462
Plant J. 2004 Nov;40(3):428-38
15469500
BMC Evol Biol. 2008 Apr 22;8:115
18430232
J Biol Chem. 2004 May 28;279(22):23364-75
15039433
Plant Signal Behav. 2008 May;3(5):320-1
19841658
Plant Cell. 2007 Jun;19(6):1930-46
17586658
Mol Biol Cell. 2001 Aug;12(8):2534-45
11514633
BMC Cell Biol. 2005 Dec 08;6:45
16336664
Plant Cell Physiol. 2005 Oct;46(10):1690-703
16100394
Biochim Biophys Acta. 2010 Feb;1803(2):201-6
18977251
Annu Rev Cell Dev Biol. 2001;17:159-87
11687487
PLoS One. 2009 May 29;4(5):e5744
19478943
Methods Mol Biol. 2005;286:91-102
15310915
Plant Physiol. 2003 Oct;133(2):462-9
14555774
J Cell Biol. 1992 Dec;119(6):1573-87
1469049
Plant Physiol. 2004 Dec;136(4):3968-78
15557099
J Cell Sci. 2005 Mar 1;118(Pt 5):937-49
15713747
Mol Biol Cell. 2002 Jan;13(1):251-61
11809837
Planta. 2005 Apr;221(1):95-104
15747143
Plant Cell. 2004 Jan;16(1):257-69
14671023
J Cell Biol. 2001 Mar 5;152(5):1019-32
11238457
Plant Physiol. 2000 Jan;122(1):35-48
10631247
DNA Res. 2007 Jun 30;14(3):103-16
17573466
FEBS Lett. 2004 Jan 16;557(1-3):88-92
14741346
Plant Cell. 1999 Dec;11(12):2349-63
10590163
J Cell Biol. 1999 Feb 8;144(3):483-96
9971743
J Exp Bot. 2010 Apr;61(7):1969-86
20159884
Cell. 1997 Feb 7;88(3):393-403
9039266
BMC Dev Biol. 2008 Aug 19;8:80
18713466
J Cell Sci. 2005 Feb 15;118(Pt 4):651-4
15701920
New Phytol. 2004 Jul;163(1):13-30
33873778
Plant Cell. 2005 Feb;17(2):486-501
15659626
Curr Opin Cell Biol. 2000 Feb;12(1):72-8
10679353
Plant Cell. 1997 Nov;9(11):1999-2010
12237353
J Biol Chem. 2000 Feb 25;275(8):5504-11
10681529
Plant J. 2007 Nov;52(3):460-72
17877706
Bioessays. 2003 Feb;25(2):152-62
12539241
Cell Motil Cytoskeleton. 2009 Nov;66(11):940-57
19504571
J Biol Chem. 1997 Oct 24;272(43):27484-91
9341203
Plant Cell. 1999 Sep;11(9):1731-42
10488239
J Biol Chem. 2007 Nov 16;282(46):33599-33608
17827159
Planta. 2000 Apr;210(5):836-43
10805457
Biochem Biophys Res Commun. 2009 Mar 13;380(3):484-8
19284992
Genetics. 1996 Feb;142(2):587-602
8852856
Mol Cell Biol. 2009 Nov;29(22):6046-58
19752190
Plant J. 1998 Nov;16(3):393-401
9881160
Mol Plant. 2008 Jul;1(4):686-702
19825573
J Biol Chem. 1998 Apr 24;273(17):10530-7
9553112