Abstract
The Antirrhinum S-locus F-box gene, AhSLF-S 2, has been shown to determine the pollen function of S-RNase-mediated self-incompatibility (SI). Its initial identification led to the discovery of a large family of plant-specific F-box proteins, named the SLF (S-Locus F-box) family, including members from species with or without S-RNase SI system. To investigate the evolution and function of its family members in Arabidopsis, we first identified 92 Arabidopsis F-box proteins related to AhSLF-S2, referred to as AtSFL (S-locus F-box-like) in this report. Phylogenetic analyses with family members from several plant species revealed that they could be classified into five subgroups, and the SLF genes appeared to have had a monophyletic origin. Yeast two-hybrid analyses showed that most AtSFL proteins could interact with one or more ASK (Arabidopsis Skp1-like) proteins, a component of the SCF (Skp1/Cullin or CDC53/F-box) complex, suggesting that AtSFLs may function in the process of ubiquitin/26S proteasome-mediated proteolysis. Transcript analysis found that most of AtSFL genes are expressed ubiquitously and only three of them (AtSFL61, 79 and 85) displayed a tissue-specific pattern. In consistent, phenotypic observations for T-DNA insertion lines of 37 AtSFL genes revealed that most of them are functionally redundant, but inactivation of two AtSFL genes (AtSFL 61 and 70) appears to have caused developmental defects in embryo or female gametophyte. Our results show that a diversified expression and functional pattern are associated with AtSFL genes, indicating that they play important roles in various biological processes in Arabidopsis.
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D. Alabadi M.J. Yanovsky P. Mas S.L. Harmer S.A. Kay (2002) ArticleTitleCritical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis Curr. Biol. 12 757–761 Occurrence Handle10.1016/S0960-9822(02)00815-1 Occurrence Handle1:CAS:528:DC%2BD38XjsFygtbo%3D Occurrence Handle12007421
Arabidopsis Genome Initiative 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815
C. Bai P. Sen K. Hofmann L. Ma M. Goebl J.W. Harper S.J. Elledge (1996) ArticleTitleSKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box Cell 86 263–274 Occurrence Handle10.1016/S0092-8674(00)80098-7 Occurrence Handle1:CAS:528:DyaK28Xks1Gns7s%3D Occurrence Handle8706131
P.A. Bariola C.J. Howard C.B. Taylor M.T. Verburg V.D. Jaglan P.J. Green (1994) ArticleTitleThe Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation Plant J. 6 673–685 Occurrence Handle1:CAS:528:DyaK2MXis1Sntbk%3D Occurrence Handle8000425
N. Bechtold G. Pelletier (1998) ArticleTitleIn planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration Methods Mol. Biol. 82 259–266 Occurrence Handle1:CAS:528:DyaK1cXjslCmt74%3D Occurrence Handle9664431
J.S. Chandler B. McArdle J. Callis (1997) ArticleTitleAtUBP3 and AtUBP4 are two closely related Arabidopsis thaliana ubiquitin-specific proteases present in the nucleus Mol. Gen. Genet. 255 302–310 Occurrence Handle10.1007/s004380050501 Occurrence Handle1:CAS:528:DyaK2sXlsFerurs%3D Occurrence Handle9268021
R.J. Deshaies (1999) ArticleTitleSCF and Cullin/RING H2-based ubiquitin ligases Annu. Rev. Cell Dev. Biol. 15 435–467 Occurrence Handle10.1146/annurev.cellbio.15.1.435 Occurrence Handle1:CAS:528:DC%2BD3cXhtVSnu74%3D Occurrence Handle10611969
T. Entani M. Iwano H. Shiba F.S. Che A. Isogai S. Takayama (2003) ArticleTitleComparative analysis of the self-incompatibility (S-) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity Genes Cells 8 203–213 Occurrence Handle10.1046/j.1365-2443.2003.00626.x Occurrence Handle1:CAS:528:DC%2BD3sXitlOjt7o%3D Occurrence Handle12622718
R. Farras A. Ferrando J. Jasik T. Kleinow L. Okresz A. Tiburcio K. Salchert C. del Pozo J. Schell C. Koncz (2001) ArticleTitleSKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase EMBO J. 20 2742–2756 Occurrence Handle10.1093/emboj/20.11.2742 Occurrence Handle1:CAS:528:DC%2BD3MXksFGrsb0%3D Occurrence Handle11387208
J.M. Gagne B.P. Downes S.H. Shiu A.M. Durski R.D. Vierstra (2002) ArticleTitleThe F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis Proc. Natl. Acad. Sci. USA 99 11519–11524 Occurrence Handle10.1073/pnas.162339999 Occurrence Handle1:CAS:528:DC%2BD38XmslSls7g%3D Occurrence Handle12169662
W.M. Gray S. Kepinski D. Rouse O. Leyser M. Estelle (2001) ArticleTitleAuxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins Nature 414 271–276 Occurrence Handle10.1038/35104500 Occurrence Handle1:CAS:528:DC%2BD3MXovFaqtb4%3D Occurrence Handle11713520
H. Guo J.R. Ecker (2003) ArticleTitlePlant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor Cell 115 667–677 Occurrence Handle10.1016/S0092-8674(03)00969-3 Occurrence Handle1:CAS:528:DC%2BD3sXhtVWgurfO Occurrence Handle14675532
R.A. Gutiérrez P.J. Green K. Keegstra J.B. Ohlrogge (2004) ArticleTitlePhylogenetic profiling of the Arabidopsis thaliana proteome: what proteins distinguish plants from other organisms? Genome Biol. 5 R53 Occurrence Handle10.1186/gb-2004-5-8-r53 Occurrence Handle15287975
E. Harlow D. Lane (1988) Antibodies: A Laboratory Manual Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 349
J.M. Herr SuffixJr. (1971) ArticleTitleA new clearing squash technique for the study of ovule development in angiosperms Am. J. Bot. 58 894–790
A. Hershko A. Ciechanover (1998) ArticleTitleThe ubiquitin system Annu. Rev. Biochem. 67 425–479 Occurrence Handle10.1146/annurev.biochem.67.1.425 Occurrence Handle1:CAS:528:DyaK1cXlsFOmsLc%3D Occurrence Handle9759494
B. Igic J.R. Kohn (2001) ArticleTitleEvolutionary relationships among self-incompatibility RNases Proc. Natl. Acad. Sci. USA 98 13167–13171 Occurrence Handle10.1073/pnas.231386798 Occurrence Handle1:CAS:528:DC%2BD3MXosFygsbY%3D Occurrence Handle11698683
H.S. Kim T.P. Delaney (2002) ArticleTitleArabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance Plant Cell 14 1469–1482 Occurrence Handle10.1105/tpc.001867 Occurrence Handle1:CAS:528:DC%2BD38XlvV2rsLY%3D Occurrence Handle12119368
Kipreos, E.T. and Pagano, M. 2000. The F-box protein family. Genome Biol. 1: reviews 3002.1–3002.7
H. Kuroda N. Takahashi H. Shimada M. Seki K. Shinozaki M. Matsui (2002) ArticleTitleClassification and expression analysis of Arabidopsis F-box-containing protein genes Plant Cell Physiol. 43 1073–1085 Occurrence Handle10.1093/pcp/pcf151 Occurrence Handle1:CAS:528:DC%2BD38Xot12htL8%3D Occurrence Handle12407186
Z. Lai W. Ma B. Han L. Liang Y. Zhang G. Hong Y. Xue (2002) ArticleTitleAn F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum Plant Mol. Biol. 50 29–42 Occurrence Handle10.1023/A:1016050018779 Occurrence Handle1:CAS:528:DC%2BD38XkslKltLg%3D Occurrence Handle12139007
Y. Liu N. Mitsukawa T. Oosumi R.F. Whittier (1995) ArticleTitleEfficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR Plant J. 8 457–463 Occurrence Handle10.1046/j.1365-313X.1995.08030457.x Occurrence Handle1:CAS:528:DyaK2MXos1CltL8%3D Occurrence Handle7550382
S.G. Mansfield L.G. Briarty (1991) ArticleTitleEarly embryogenesis in Arabidopsis thaliana: 1. The developing embryo Can. J. Bot. 69 461–476
P. Mas W.Y. Kim D.E. Somers S.A. Kay (2003) ArticleTitleTargeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana Nature 26 567–570 Occurrence Handle10.1038/nature02163
K.M. McGinnis S.G. Thomas J.D. Soule L.C. Strader J.M. Zale T.P. Sun C.M. Steber (2003) ArticleTitleThe Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase Plant Cell 15 1120–1130 Occurrence Handle10.1105/tpc.010827 Occurrence Handle1:CAS:528:DC%2BD3sXjvV2htLY%3D Occurrence Handle12724538
E.E. Patton A.R. Willems M. Tyers (1998) ArticleTitleCombinatorial control ubiquitin-dependent proteolysis: don’t Skp the F-box hypothesis Trends Genet. 14 236–243 Occurrence Handle10.1016/S0168-9525(98)01473-5 Occurrence Handle1:CAS:528:DyaK1cXjslanur4%3D Occurrence Handle9635407
T. Potuschak E. Lechner Y. Parmentier S. Yanagisawa S. Grava C. Koncz P. Genschik (2003) ArticleTitleEIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F- box proteins: EBF1 and EBF2 Cell 115 679–689 Occurrence Handle10.1016/S0092-8674(03)00968-1 Occurrence Handle1:CAS:528:DC%2BD3sXhtVWgurfP Occurrence Handle14675533
J.A. Printen G.F. Sprague SuffixJr. (1994) ArticleTitleProtein interactions in yeast pheromoneresponse pathway: Ste5p interacts with all members of the MAP kinase cascade Genetics 138 609–619 Occurrence Handle1:CAS:528:DyaK28XitlKjtg%3D%3D Occurrence Handle7851759
H. Qiao H. Wang L. Zhao J. Zhou J. Huang Y. Zhang Y. Xue (2004b) ArticleTitleThe F-Box protein AhSLF-S2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S proteasome pathway of protein degradation during compatible pollination in Antirrhinum Plant Cell 16 582–595 Occurrence Handle10.1105/tpc.017673 Occurrence Handle1:CAS:528:DC%2BD2cXisFGkt70%3D
H. Qiao F. Wang L. Zhao J. Zhou Z. Lai Y. Zhang T.P. Robbins Y. Xue (2004a) ArticleTitleThe F-Box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility Plant Cell 16 2307–2332 Occurrence Handle10.1105/tpc.104.024919 Occurrence Handle1:CAS:528:DC%2BD2cXnvVartLg%3D
E.P. Risseeuw T.E. Daskalchuk T.W. Banks E. Liu S.L. Cotelesage H. Hellmann M. Estelle D.E. Somer W.L. Crosby (2003) ArticleTitleProtein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis Plant J. 34 753–767 Occurrence Handle10.1046/j.1365-313X.2003.01768.x Occurrence Handle1:CAS:528:DC%2BD3sXlvFajsLo%3D Occurrence Handle12795696
K. Sakata Y. Nagamura H. Numa B.A. Antonio H. Nagasaki A. Idonuma W. Watanabe Y. Shimizu I. Horiuchi T. Matsumoto T. Sasaki K. Higo (2002) ArticleTitleRiceGAAS: an automated annotation system and database for rice genome sequence Nucleic Acids Res. 30 98–102 Occurrence Handle10.1093/nar/30.1.98 Occurrence Handle1:CAS:528:DC%2BD38Xht12kt7s%3D Occurrence Handle11752265
K. Sato T. Nishio R. Kimura M. Kusaba T. Suzuki K. Hatakeyama D.J. Ockendon Y. Satta (2002) ArticleTitleCoevolution of the S-locus genes SRK, SLG and SP11/SCR in Brassica oleracea and B. rapa Genetics 162 931–940 Occurrence Handle1:CAS:528:DC%2BD38XptVOrtrg%3D Occurrence Handle12399400
G. Serino T. Tsuge S. Kwok M. Matsui N. Wei X.W. Deng (1999) ArticleTitleArabidopsiscop8 and fus4 mutations define the same gene that encodes subunit 4 of the COP9 signalosome Plant Cell 11 1967–1980 Occurrence Handle10.1105/tpc.11.10.1967 Occurrence Handle1:CAS:528:DyaK1MXntFCgtLo%3D Occurrence Handle10521526
P. Sijacic X. Wang A.L. Skirpan Y. Wang P.E. Dowd A.G. McCubbin S. Huang T.H. Kao (2004) ArticleTitleIdentification of the pollen determinant of S-RNase-mediated self-incompatibility Nature 429 302–305 Occurrence Handle10.1038/nature02523 Occurrence Handle1:CAS:528:DC%2BD2cXktVOqtb0%3D Occurrence Handle15152253
J. Smalle R.D. Vierstra (2004) ArticleTitleThe ubiquitin 26S proteasome proteolytic pathway Annu. Rev. Plant Biol. 55 555–590 Occurrence Handle10.1146/annurev.arplant.55.031903.141801 Occurrence Handle1:CAS:528:DC%2BD2cXlvFeisb4%3D Occurrence Handle15377232
D.E. Somers T.F. Schultz M. Milnamow S.A. Kay (2000) ArticleTitleZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis Cell 101 319–329 Occurrence Handle10.1016/S0092-8674(00)80841-7 Occurrence Handle1:CAS:528:DC%2BD3cXjtFSrtLg%3D Occurrence Handle10847686
J.A. Sullivan K. Shirasu X.W. Deng (2003) ArticleTitleThe diverse roles of ubiquitin and the 26s proteasome in the life of plants Nat. Rev. Genet. 4 948–958 Occurrence Handle10.1038/nrg1228 Occurrence Handle1:CAS:528:DC%2BD3sXptFait7c%3D Occurrence Handle14631355
N. Takahashi H. Kuroda T. Kuromori T. Hirayama M. Seki K. Shinozaki H. Shimada M. Matsui (2004) ArticleTitleExpression and interaction analysis of Arabidopsis Skp1-related genes Plant Cell Physiol. 45 83–91 Occurrence Handle10.1093/pcp/pch009 Occurrence Handle1:CAS:528:DC%2BD2cXpsVaitw%3D%3D Occurrence Handle14749489
C.B. Taylor P.A. Bariola S.B. del Cardayré R.T. Raines P.J. Green (1993) ArticleTitleRNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation Proc. Natl. Acad. Sci. USA 90 5118–5112 Occurrence Handle1:CAS:528:DyaK3sXkvFSjsL4%3D Occurrence Handle8506358
K. Ushijima H. Sassa A.M. Dandekar T.M. Gradziel R. Tao H. Hirano (2003) ArticleTitleStructural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism Plant Cell 15 771–781 Occurrence Handle10.1105/tpc.009290 Occurrence Handle1:CAS:528:DC%2BD3sXisVektbo%3D Occurrence Handle12615948
K. Ushijima H. Yamane A. Watari E. Kakehi K. Ikeda N.R. Hauck A.F. Iezzoni R. Tao (2004) ArticleTitleThe S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume Plant J. 39 573–586 Occurrence Handle10.1111/j.1365-313X.2004.02154.x Occurrence Handle1:CAS:528:DC%2BD2cXnslOmsro%3D Occurrence Handle15272875
H. Wang J. Huang Z. Lai Y. Xue (2002) ArticleTitleF-box proteins in flowering plants Chin. Sci. Bull. 47 1497–1501 Occurrence Handle10.1360/02tb9330 Occurrence Handle1:CAS:528:DC%2BD38XnvFyju7g%3D
Y. Wang T. Tsukamoto K.W. Yi X. Wang S. Huang A.G. McCubbin T.H. Kao (2004) ArticleTitleChromosome walking in the Putunia inflate self-incompatibility (S-) locus and gene identification in a 881-kb contig containing S 2-RNase Plant Mol. Biol. 54 727–742 Occurrence Handle10.1023/B:PLAN.0000040901.98982.82 Occurrence Handle1:CAS:528:DC%2BD2cXptlCrtLk%3D Occurrence Handle15356391
Y. Wang X. Wang A.G. McCubbin T.H. Kao (2003) ArticleTitleGenetic mapping and molecular characterization of the self-incompatibility (S) locus in Petunia inflata Plant Mol. Biol. 53 565–580 Occurrence Handle10.1023/B:PLAN.0000019068.00034.09 Occurrence Handle1:CAS:528:DC%2BD2cXhvFCgt74%3D Occurrence Handle15010619
D. Weigel J. Galzebrook (2002) Arabidopsis: A Laboratory Manual Cold Spring Harbor Laboratory Press Cold Spring Harbor NY 243–248
J.T. Winston D.M. Koepp C. Zhu S.J. Elledge J.W. Harper (1999) ArticleTitleA family of mammalian F-box proteins Curr. Biol. 9 1180–1182 Occurrence Handle10.1016/S0960-9822(00)80021-4 Occurrence Handle1:CAS:528:DyaK1MXntVSlt7s%3D Occurrence Handle10531037
Y. Xue R. Carpenter H.G. Dickinson E.S. Coen (1996) ArticleTitleOrigin of allelic diversity in Antirrhinum S locus RNases Plant Cell 8 805–814 Occurrence Handle10.1105/tpc.8.5.805 Occurrence Handle1:CAS:528:DyaK28XjtlOksbs%3D Occurrence Handle8672882
H. Yamane K. Ikeda K. Ushijima H. Sassa R. Tao (2003) ArticleTitleA pollen-expressed gene for a novel protein with an F-box motif that is very tightly linked to a gene for S-RNase in two species of cherry, Prunus cerasus and P. avium Plant Cell Physiol. 44 764–769 Occurrence Handle10.1093/pcp/pcg088 Occurrence Handle1:CAS:528:DC%2BD3sXlslGmu70%3D Occurrence Handle12881505
J. Zhou F. Wang W. Ma Y. Zhang B. Han Y. Xue (2003) ArticleTitleStructural and transcriptional analysis of S-Locus F-box genes in Antirrhinum Sex. Plant Reprod. 16 165–177 Occurrence Handle10.1007/s00497-003-0185-5 Occurrence Handle1:CAS:528:DC%2BD3sXosVGjurg%3D
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Wang, L., Dong, L., Zhang, Y. et al. Genome-wide analysis of S-Locus F-box-like genes in Arabidopsis thaliana . Plant Mol Biol 56, 929–945 (2004). https://doi.org/10.1007/s11103-004-6236-y
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DOI: https://doi.org/10.1007/s11103-004-6236-y