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An Auxin-Inducible F-Box Protein CEGENDUO Negatively Regulates Auxin-Mediated Lateral Root Formation in Arabidopsis

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Abstract

Previously, we characterized 92 Arabidopsis genes (AtSFLs) similar to the S-locus F-box genes involved in S-RNase-based self-incompatibility and found that they likely play diverse roles in Arabidopsis. In this study, we investigated the role of one of these genes, CEGENDUO (CEG, AtSFL61), in the lateral root formation. A T-DNA insertion in CEG led to an increased lateral root production, which was complemented by transformation of the wild-type gene. Its downregulation by RNAi also produced more lateral roots in transformed Arabidopsis plants whereas its overexpression generated less lateral roots compared to wild-type, indicating that CEG acts as a negative regulator for the lateral root formation. It was found that CEG was expressed abundantly in vascular tissues of the primary root, but not in newly formed lateral root primordia and the root meristem, and induced by exogenous auxin NAA (α-naphthalene acetic acid). In addition, the ceg mutant was hyposensitive to NAA, IAA (indole-3-acetic acid) and 2,4-D (2,4-dichlorophenoxyacetic acid), as well as the auxin transport inhibitor TIBA (3,3,5-triiodobenzoic acid), showing that CEG is an auxin-inducible gene. Taken together, our results show that CEG is a novel F-box protein negatively regulating the auxin-mediated lateral root formation in Arabidopsis.

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References

  • 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

    CAS  PubMed  Google Scholar 

  • Y. Ben-Neriah (2002) ArticleTitleRegulatory functions of ubiquitination in the immune system Nat. Immunol. 3 20–26 Occurrence Handle10.1038/ni0102-20 Occurrence Handle1:CAS:528:DC%2BD38XktlCmtQ%3D%3D Occurrence Handle11753406

    Article  CAS  PubMed  Google Scholar 

  • R.P. Bhalerao J. Eklof K. Ljung A. Marchant M. Bennett G. Sandberg (2002) ArticleTitleShoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings Plant J. 29 325–332 Occurrence Handle10.1046/j.0960-7412.2001.01217.x Occurrence Handle1:CAS:528:DC%2BD38XhvFOitL8%3D Occurrence Handle11844109

    Article  CAS  PubMed  Google Scholar 

  • JL. Celenza SuffixJr. P.L. Grisafi G.R. Fink (1995) ArticleTitleA pathway for lateral root formation in Arabidopsis thaliana Genes Dev. 9 2131–2142 Occurrence Handle1:CAS:528:DyaK2MXotVOnu7o%3D Occurrence Handle7657165

    CAS  PubMed  Google Scholar 

  • A. Ciechanover (1998) ArticleTitleThe ubiquitin-proteasome pathway: on protein death and cell life EMBO J. 17 7151–7160 Occurrence Handle10.1093/emboj/17.24.7151 Occurrence Handle1:CAS:528:DyaK1MXktl2hsQ%3D%3D Occurrence Handle9857172

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • N. Dharmasiri S. Dharmasiri M. Estelle (2005) ArticleTitleThe F-box protein TIR1 is an auxin receptor Nature 435 IssueID7041 441–445 Occurrence Handle10.1038/nature03543 Occurrence Handle1:CAS:528:DC%2BD2MXksVeisrs%3D Occurrence Handle15917797

    Article  CAS  PubMed  Google Scholar 

  • L. Dolan K. Janmaat V. Willemsen P. Linstead S. Poethig K. Roberts B. Scheres (1993) ArticleTitleCellular organisation of the Arabidopsis thaliana root Development 119 71–84 Occurrence Handle1:STN:280:ByuC3c3gsFQ%3D Occurrence Handle8275865

    CAS  PubMed  Google Scholar 

  • H. Fukaki S. Tameda H. Masuda M. Tasaka (2002) ArticleTitleLateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis Plant J. 29 153–168 Occurrence Handle10.1046/j.0960-7412.2001.01201.x Occurrence Handle1:CAS:528:DC%2BD38XhvF2qtLk%3D Occurrence Handle11862947

    Article  CAS  PubMed  Google Scholar 

  • S.R. Gallagher (1992) Quantitation of GUS activity by flurometry S.R. Gallagher (Eds) GUS Protocols; Using the GUS Gene as a Reporter of Gene expression Academic Press New York

    Google Scholar 

  • N. Geldner J. Friml Y.D. Stierhof G. Jurgens K. Palme (2001) ArticleTitleAuxin transport inhibitors block PIN1 cycling and vesicle trafficking Nature 413 IssueID6854 425–428 Occurrence Handle10.1038/35096571 Occurrence Handle1:CAS:528:DC%2BD3MXntl2gtb0%3D Occurrence Handle11574889

    Article  CAS  PubMed  Google Scholar 

  • W.M. Gray J.C. Pozo Particledel L. Walker L. Hobbie E. Risseeuw T. Banks W.L. Crosby M. Yang H. Ma M. Estelle (1999) ArticleTitleIdentification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana Genes Dev. 13 IssueID13 1678–1691 Occurrence Handle1:CAS:528:DyaK1MXkvVCku7k%3D Occurrence Handle10398681

    CAS  PubMed  Google Scholar 

  • W.M. Gray S. Kepinski D. Rouse O. Leyser M. Estelle (2001) ArticleTitleAuxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins Nature 414 IssueID6861 271–276 Occurrence Handle10.1038/35104500 Occurrence Handle1:CAS:528:DC%2BD3MXovFaqtb4%3D Occurrence Handle11713520

    Article  CAS  PubMed  Google Scholar 

  • H.S. Guo Q. Xie J.F. Fei N.H. Chua (2005) ArticleTitleMicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development Plant Cell 17 IssueID5 1376–1386 Occurrence Handle10.1105/tpc.105.030841 Occurrence Handle1:CAS:528:DC%2BD2MXksVKksrk%3D Occurrence Handle15829603

    Article  CAS  PubMed  Google Scholar 

  • N.P. Hawker J.L. Bowman (2004) ArticleTitleRoles for class III HD-Zip and KANADI genes in Arabidopsis root development Plant Physiol. 135 IssueID4 2261–2270 Occurrence Handle10.1104/pp.104.040196 Occurrence Handle1:CAS:528:DC%2BD2cXnt1GgsLg%3D Occurrence Handle15286295

    Article  CAS  PubMed  Google Scholar 

  • K. Himanen E. Boucheron S. Vanneste J. Almeida Engler Particlede D. Inze T. Beeckman (2002) ArticleTitleAuxin-mediated cell cycle activation during early lateral root initiation Plant Cell 14 2339–2351 Occurrence Handle10.1105/tpc.004960 Occurrence Handle1:CAS:528:DC%2BD38XotFels70%3D Occurrence Handle12368490

    Article  CAS  PubMed  Google Scholar 

  • L. Hobbie M. Estelle (1995) ArticleTitleThe axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation Plant J. 7 211–220 Occurrence Handle10.1046/j.1365-313X.1995.7020211.x Occurrence Handle1:CAS:528:DyaK2MXkslGnt7g%3D Occurrence Handle7704045

    Article  CAS  PubMed  Google Scholar 

  • S. Kepinski O. Leyser (2004) ArticleTitleAuxin-induced SCFTIR1-AUX/IAA interaction involves stable modification of the SCFTIR1 complex Proc Natl Acad Sci USA. 101 IssueID33 12381–12386 Occurrence Handle10.1073/pnas.0402868101 Occurrence Handle1:CAS:528:DC%2BD2cXntFektb0%3D Occurrence Handle15295098

    Article  CAS  PubMed  Google Scholar 

  • S. Kepinski O. Leyser (2005) ArticleTitleThe Arabidopsis F-box protein TIR1 is an auxin receptor Nature 435 IssueID7041 446–451 Occurrence Handle10.1038/nature03542 Occurrence Handle1:CAS:528:DC%2BD2MXksVeisro%3D Occurrence Handle15917798

    Article  CAS  PubMed  Google Scholar 

  • 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 Handle1:CAS:528:DC%2BD38XlvV2rsLY%3D Occurrence Handle12119368

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • M.J. Laskowski M.E. Williams H.C. Nusbaum I.M. Sussex (1995) ArticleTitleFormation of lateral root meristems is a two-stage process Development 121 3303–3310 Occurrence Handle1:CAS:528:DyaK2MXptV2hsbw%3D Occurrence Handle7588064

    CAS  PubMed  Google Scholar 

  • R. Lin H. Wang (2005) ArticleTitleTwo homologous ATP-binding cassette transporter proteins, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport Plant Physiol. 138 IssueID2 949–964 Occurrence Handle10.1104/pp.105.061572 Occurrence Handle1:CAS:528:DC%2BD2MXmtVejs7s%3D Occurrence Handle15908594

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • A.C. Mallory D.V. Dugas D.P. Bartel B. Bartel (2004) ArticleTitleMicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs Curr. Biol. 14 1035–1046 Occurrence Handle10.1016/j.cub.2004.06.022 Occurrence Handle1:CAS:528:DC%2BD2cXltVOgtLg%3D Occurrence Handle15202996

    Article  CAS  PubMed  Google Scholar 

  • J. Moon G. Parry M. Estelle (2004) ArticleTitleThe ubiquitin-proteasome pathway and plant development Plant Cell 16 3181–3195 Occurrence Handle10.1105/tpc.104.161220 Occurrence Handle1:CAS:528:DC%2BD2MXhtVKnug%3D%3D Occurrence Handle15579807

    Article  CAS  PubMed  Google Scholar 

  • L.A. Nodzon W. Xu Y. Wang L. Pi P.K. Chakrabarty W.Y. Song (2004) ArticleTitleThe ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis Plant J. 40 IssueID6 996–1006 Occurrence Handle10.1111/j.1365-313X.2004.02266.x Occurrence Handle1:CAS:528:DC%2BD2MXpslGgsg%3D%3D Occurrence Handle15584963

    Article  CAS  PubMed  Google Scholar 

  • Y. Okushima P.J. Overvoorde K. Arima J.M. Alonso A. Chan C Chang J.R. Ecker B. Hughes A. Lui D. Nguyen C. Onodera H. Quach A. Smith G. Yu A. Theologis (2005) ArticleTitleFunctional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19 Plant Cell 17 444–463 Occurrence Handle10.1105/tpc.104.028316 Occurrence Handle1:CAS:528:DC%2BD2MXhsFKqsro%3D Occurrence Handle15659631

    Article  CAS  PubMed  Google Scholar 

  • T. Oyama Y. Shimura K. Okada (1997) ArticleTitleThe Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl Genes Dev. 11 2983–2995 Occurrence Handle1:CAS:528:DyaK2sXns1altbs%3D Occurrence Handle9367981

    CAS  PubMed  Google Scholar 

  • 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 Handle1:CAS:528:DC%2BD2cXnvVartLg%3D

    CAS  Google Scholar 

  • 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 Handle1:CAS:528:DC%2BD2cXisFGkt70%3D

    CAS  Google Scholar 

  • J.W. Reed (2001) ArticleTitleRoles and activities of AUX/IAA proteins in Arabidopsis Trends Plant Sci. 6 420–425 Occurrence Handle10.1016/S1360-1385(01)02042-8 Occurrence Handle1:CAS:528:DC%2BD3MXmvF2hur0%3D Occurrence Handle11544131

    Article  CAS  PubMed  Google Scholar 

  • D.L. Remington T.J. Vision T.J. Guilfoyle J.W. Reed (2004) ArticleTitleContrasting modes of diversification in the Aux/IAA and ARF gene families Plant Physiol. 135 1738–1752 Occurrence Handle10.1104/pp.104.039669 Occurrence Handle1:CAS:528:DC%2BD2cXmtVOqsbc%3D Occurrence Handle15247399

    Article  CAS  PubMed  Google Scholar 

  • M.W. Rhoades B.J. Reinhart L.P. Lim C.B. Burge B. Bartel D.P. Bartel (2002) ArticleTitlePrediction of plant microRNA targets Cell 110 513–520 Occurrence Handle10.1016/S0092-8674(02)00863-2 Occurrence Handle1:CAS:528:DC%2BD38Xmslyjt7s%3D Occurrence Handle12202040

    Article  CAS  PubMed  Google Scholar 

  • L.E. Rogg J. Lasswell B. Bartel (2001) ArticleTitleA gain-of-function mutation in IAA28 suppresses lateral root development Plant Cell 13 465–480 Occurrence Handle10.1105/tpc.13.3.465 Occurrence Handle1:CAS:528:DC%2BD3MXis1aksbY%3D Occurrence Handle11251090

    Article  CAS  PubMed  Google Scholar 

  • M. Ruegger E. Dewey W.M. Gray L. Hobbie J. Turner M. Estelle (1998) ArticleTitleThe TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p Genes Dev. 12 198–207 Occurrence Handle1:CAS:528:DyaK1cXnsV2iug%3D%3D Occurrence Handle9436980

    CAS  PubMed  Google Scholar 

  • M. Ruegger E. Dewey L. Hobbie D. Brown P. Bernasconi J. Turner G. Muday M. Estelle (1997) ArticleTitleReduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects Plant Cell 9 745–757 Occurrence Handle10.1105/tpc.9.5.745 Occurrence Handle1:CAS:528:DyaK2sXjtlejsLs%3D Occurrence Handle9165751

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • H. Stals D. Inze (2001) ArticleTitleWhen plant cells decide to divide Trends Plant Sci. 6 359–364 Occurrence Handle10.1016/S1360-1385(01)02016-7 Occurrence Handle1:CAS:528:DC%2BD3MXmtFCktLg%3D Occurrence Handle11495789

    Article  CAS  PubMed  Google Scholar 

  • K. Tatematsu S. Kumagai H. Muto A. Sato M.K. Watahiki R.M. Harper E. Liscum K.T. Yamamoto (2004) ArticleTitleMASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana Plant Cell 16 379–393 Occurrence Handle10.1105/tpc.018630 Occurrence Handle1:CAS:528:DC%2BD2cXhsFKis70%3D Occurrence Handle14729917

    Article  CAS  PubMed  Google Scholar 

  • Q. Tian J.W. Reed (1999) ArticleTitleControl of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene Development 126 711–721 Occurrence Handle1:CAS:528:DyaK1MXhvFamsLo%3D Occurrence Handle9895319

    CAS  PubMed  Google Scholar 

  • T. Ulmasov G. Hagen T.J. Guilfoyle (1997a) ArticleTitleARF1, a transcriptional factor that binds to auxin response elements Science 276 1865–1868 Occurrence Handle10.1126/science.276.5320.1865 Occurrence Handle1:CAS:528:DyaK2sXksVCnu7k%3D

    Article  CAS  Google Scholar 

  • T. Ulmasov J. Murfett G. Hagen T.J. Guilfoyle (1997b) ArticleTitleAUX/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements Plant Cell 9 1963–1971 Occurrence Handle10.1105/tpc.9.11.1963 Occurrence Handle1:CAS:528:DyaK2sXnsl2mtrc%3D

    Article  CAS  Google Scholar 

  • L. Wang L. Dong Y. Zhang Y. Zhang W. Wu X. Deng Y. Xue (2004) ArticleTitleGenome-wide analysis of S-Locus F-box-like genes in Arabidopsis thaliana Plant Mol Biol. 56 IssueID6 929–945 Occurrence Handle10.1007/s11103-004-6236-y Occurrence Handle1:CAS:528:DC%2BD2MXjtV2gsLg%3D Occurrence Handle15821991

    Article  CAS  PubMed  Google Scholar 

  • D. Weigel J. Galzebrook (2002) Arabidopsis: A Laboratory Manual Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 243–248

    Google Scholar 

  • J.C. Wilmoth S. Wang S.B. Tiwari A.D. Joshi G. Hagen T.J. Guilfoyle J.M. Alonso J.R. Ecker J. Reed (2005) ArticleTitleNPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation Plant J. 43 118–130 Occurrence Handle10.1111/j.1365-313X.2005.02432.x Occurrence Handle1:CAS:528:DC%2BD2MXmsVehs70%3D Occurrence Handle15960621

    Article  CAS  PubMed  Google Scholar 

  • Q. Xie G. Frugis D. Colgan N.H. Chua (2000) ArticleTitleArabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development Genes Dev. 14 3024–3036 Occurrence Handle1:CAS:528:DC%2BD3cXptVWlt78%3D Occurrence Handle11114891

    CAS  PubMed  Google Scholar 

  • Q. Xie H.S. Guo G. Dallman S. Fang A.M. Weissman N.H. Chua (2002) ArticleTitleSINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals Nature 419 167–170 Occurrence Handle10.1038/nature00998 Occurrence Handle1:CAS:528:DC%2BD38XmvV2qsL0%3D Occurrence Handle12226665

    Article  CAS  PubMed  Google Scholar 

  • X. Yang S. Lee J.H. So S. Dharmasiri N. Dharmasiri L. Ge C. Jensen R. Hangarter L. Hobbie M. Estelle (2004) ArticleTitleThe IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1 Plant J. 40 IssueID5 772–782 Occurrence Handle10.1111/j.1365-313X.2004.02254.x Occurrence Handle1:CAS:528:DC%2BD2MXjvFWgsQ%3D%3D Occurrence Handle15546359

    Article  CAS  PubMed  Google Scholar 

  • J. Zuo Q.W. Niu S.G Moller N.H. Chua (2001) ArticleTitleChemical-regulated, site-specific DNA excision in transgenic plants Nat. Biotechnol. 19 157–161 Occurrence Handle10.1038/84428 Occurrence Handle1:CAS:528:DC%2BD3MXhtVaitLg%3D Occurrence Handle11175731

    Article  CAS  PubMed  Google Scholar 

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Dong, L., Wang, L., Zhang, Y. et al. An Auxin-Inducible F-Box Protein CEGENDUO Negatively Regulates Auxin-Mediated Lateral Root Formation in Arabidopsis. Plant Mol Biol 60, 599–615 (2006). https://doi.org/10.1007/s11103-005-5257-5

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