title: Plant WEE1 kinase is cell cycle regulated and removed at mitosis via the 26S proteasome machinery.
abstract: In yeasts and animals, premature entry into mitosis is prevented by the inhibitory phosphorylation of cyclin-dependent kinase (CDK) by WEE1 kinase, and, at mitosis, WEE1 protein is removed through the action of the 26S proteasome. Although in higher plants WEE1 function has been confirmed in the DNA replication checkpoint, Arabidopsis wee1 insertion mutants grow normally, and a role for the protein in the G2/M transition during an unperturbed plant cell cycle is yet to be confirmed. Here data are presented showing that the inhibitory effect of WEE1 on CDK activity in tobacco BY-2 cell cultures is cell cycle regulated independently of the DNA replication checkpoint: it is high during S-phase but drops as cells traverse G2 and enter mitosis. To investigate this mechanism further, a yeast two-hybrid screen was undertaken to identify proteins interacting with Arabidopsis WEE1. Three F-box proteins and a subunit of the proteasome complex were identified, and bimolecular fluorescence complementation confirmed an interaction between AtWEE1 and the F-box protein SKP1 interacting partner 1 (SKIP1). Furthermore, the AtWEE1-green fluorescent protein (GFP) signal in Arabidopsis primary roots treated with the proteasome inhibitor MG132 was significantly increased compared with mock-treated controls. Expression of AtWEE1-YFP(C) (C-terminal portion of yellow fluorescent protein) or AtWEE1 per se in tobacco BY-2 cells resulted in a premature increase in the mitotic index compared with controls, whereas co-expression of AtSKIP1-YFP(N) negated this effect. These data support a role for WEE1 in a normal plant cell cycle and its removal at mitosis via the 26S proteasome.
authors.affiliation: School of Biosciences, Cardiff University, Main Building, Park Place, Cardiff CF10 3TL, UK.
authors.forename: Gemma S
authors.initials: GS
authors.lastname: Cook
authors.forename: Anne Lentz
authors.initials: AL
authors.lastname: Grønlund
authors.forename: Ilario
authors.initials: I
authors.lastname: Siciliano
authors.forename: Natasha
authors.initials: N
authors.lastname: Spadafora
authors.forename: Maryam
authors.initials: M
authors.lastname: Amini
authors.forename: Robert J
authors.initials: RJ
authors.lastname: Herbert
authors.forename: M Beatrice
authors.initials: MB
authors.lastname: Bitonti
authors.forename: Katja
authors.initials: K
authors.lastname: Graumann
authors.forename: Dennis
authors.initials: D
authors.lastname: Francis
authors.forename: Hilary J
authors.initials: HJ
authors.lastname: Rogers
mesh_terms: D017360:Arabidopsis / Q000166:cytology / Q000201:enzymology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D002453:Cell Cycle / Q000235:genetics / Q000502:physiology*; D008938:Mitosis; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D046988:Proteasome Endopeptidase Complex / Q000235:genetics / Q000378:metabolism*; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism*; D014026:Nicotiana / Q000166:cytology / Q000201:enzymology
chemical_list: D029681:Arabidopsis Proteins; D010940:Plant Proteins; D017346:Protein Serine-Threonine Kinases; C514674:WEE1 protein, Arabidopsis; D046988:Proteasome Endopeptidase Complex; C061553:ATP dependent 26S protease
references.citation: EMBO J. 1995 May 15;14(10):2166-75
references.pmid: 7774574
references.citation: Genes Dev. 1998 Aug 15;12(16):2587-97
references.pmid: 9716410
references.citation: Plant J. 1998 Dec;16(6):735-43
references.pmid: 10069079
references.citation: Mol Cell. 2002 May;9(5):931-43
references.pmid: 12049731
references.citation: Trends Plant Sci. 2006 Oct;11(10):474-9
references.pmid: 16949857
references.citation: Plant J. 2008 Nov;56(3):505-16
references.pmid: 18643980
references.citation: Plant Cell. 2004 Mar;16(3):643-57
references.pmid: 15004270
references.citation: Nature. 2002 Apr 18;416(6882):703-9
references.pmid: 11961546
references.citation: Plant Mol Biol. 2004 Dec;56(6):849-61
references.pmid: 15821985
references.citation: Nat Rev Genet. 2003 Dec;4(12):948-58
references.pmid: 14631355
references.citation: Cell. 1995 Apr 21;81(2):279-88
references.pmid: 7736580
references.citation: Planta. 2002 Jul;215(3):518-22
references.pmid: 12111237
references.citation: PLoS One. 2010 Dec 06;5(12):e15089
references.pmid: 21151918
references.citation: Plant Cell. 2007 Jan;19(1):211-25
references.pmid: 17209125
references.citation: Nature. 1990 Apr 5;344(6266):503-8
references.pmid: 2138713
references.citation: Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4180-5
references.pmid: 10097184
references.citation: Plant Cell. 1998 Dec;10(12):2063-76
references.pmid: 9836745
references.citation: Plant Physiol. 1985 Oct;79(2):568-70
references.pmid: 16664453
references.citation: Anal Biochem. 1976 May 7;72:248-54
references.pmid: 942051
references.citation: Ann Bot. 2012 Dec;110(8):1631-9
references.pmid: 23065633
references.citation: Plant J. 2004 Nov;40(3):428-38
references.pmid: 15469500
references.citation: Plant J. 2003 Jun;34(6):753-67
references.pmid: 12795696
references.citation: Plant J. 2005 Oct;44(2):290-9
references.pmid: 16212607
references.citation: Cell. 1997 Oct 17;91(2):209-19
references.pmid: 9346238
references.citation: Cell. 1994 Sep 9;78(5):761-71
references.pmid: 8087844
references.citation: BMC Plant Biol. 2009 Apr 22;9:44
references.pmid: 19386122
references.citation: Plant Mol Biol. 2000 Aug;43(5-6):607-20
references.pmid: 11089864
references.citation: Plant Cell. 2001 Mar;13(3):495-509
references.pmid: 11251092
references.citation: Planta. 2003 Nov;218(1):50-7
references.pmid: 12942327
references.citation: Int J Biol Sci. 2006;2(4):161-70
references.pmid: 16810330
references.citation: Proc Natl Acad Sci U S A. 2009 Jan 20;106(3):835-40
references.pmid: 19126682
references.citation: Plant Cell. 2011 Apr;23(4):1435-48
references.pmid: 21498679
references.citation: Plant J. 2003 May;34(4):417-25
references.pmid: 12753582
references.citation: Annu Rev Cell Dev Biol. 1999;15:435-67
references.pmid: 10611969
references.citation: Oncogene. 2005 Apr 14;24(16):2723-34
references.pmid: 15735764
references.citation: Mol Biol Evol. 2007 Aug;24(8):1596-9
references.pmid: 17488738
references.citation: Plant J. 2007 Aug;51(4):642-55
references.pmid: 17587306
references.citation: Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4419-24
references.pmid: 15070733
references.citation: Biochem J. 2011 May 1;435(3):661-7
references.pmid: 21323637
references.citation: Nature. 2000 Jun 1;405(6786):575-9
references.pmid: 10850717
references.citation: Plant J. 2009 Aug;59(4):645-60
references.pmid: 19392699
references.citation: Science. 1998 Dec 4;282(5395):1886-9
references.pmid: 9836638
references.citation: J Biol Chem. 2001 Sep 28;276(39):36354-60
references.pmid: 11477067
references.citation: Plant Physiol. 2001 Jul;126(3):1214-23
references.pmid: 11457971
references.citation: Cell. 2003 Apr 4;113(1):101-13
references.pmid: 12679038
references.citation: Cell. 1997 Oct 17;91(2):221-30
references.pmid: 9346239
references.citation: Plant J. 2010 Jan;61(1):134-44
references.pmid: 19807882