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Whorl-Specific Expression of the SUPERMAN Gene of Arabidopsis Is Mediated by cis Elements in the Transcribed Region

2003; Elsevier BV; Volume: 13; Issue: 17 Linguagem: Inglês

10.1016/s0960-9822(03)00612-2

1879-0445

Toshiro Ito, Hajime Sakai, Elliot M. Meyerowitz,

Plant nutrient uptake and metabolism

The SUPERMAN (SUP) gene of Arabidopsis is involved in controlling cell proliferation in stamen and carpel primordia and in ovules during flower development [1Schultz E.A. Pickett F.B. Haughn G.W. The flo10 gene product regulates the expression domain of homeotic genes AP3 and PI in Arabidopsis flowers.Plant Cell. 1991; 3: 1221-1237Crossref PubMed Google Scholar, 2Bowman J.L. Sakai H. Jack T. Weigel D. Mayer U. Meyerowitz E.M. SUPERMAN, a regulator of floral homeotic genes in Arabidopsis.Development. 1992; 114: 599-615Crossref PubMed Google Scholar, 3Sakai H. Medrano L.J. Meyerowitz E.M. Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries.Nature. 1995; 378: 199-203Crossref PubMed Scopus (347) Google Scholar, 4Gaiser J.C. Robinson-Beers K. Gasser C.S. The Arabidopsis SUPERMAN gene mediates asymmetric growth of the outer integument of ovules.Plant Cell. 1995; 7: 333-345Crossref PubMed Scopus (126) Google Scholar, 5Sakai H. Krizek B.A. Jacobsen S.E. Meyerowitz E.M. Regulation of SUP expression identifies multiple regulators involved in Arabidopsis floral meristem development.Plant Cell. 2000; 12: 1607-1618Crossref PubMed Scopus (85) Google Scholar]. The SUP gene encodes a transcription factor with a C2H2-type zinc finger motif, a serine/proline-rich domain, a basic domain, and a leucine-zipper-like domain and is expressed in a very limited region in stamen primordia and in the developing ovary during flower development [3Sakai H. Medrano L.J. Meyerowitz E.M. Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries.Nature. 1995; 378: 199-203Crossref PubMed Scopus (347) Google Scholar, 5Sakai H. Krizek B.A. Jacobsen S.E. Meyerowitz E.M. Regulation of SUP expression identifies multiple regulators involved in Arabidopsis floral meristem development.Plant Cell. 2000; 12: 1607-1618Crossref PubMed Scopus (85) Google Scholar]. The SUP gene is susceptible to methylation, resulting in epigenetic gene silencing [6Jacobsen S.E. Meyerowitz E.M. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis.Science. 1997; 277: 1100-1103Crossref PubMed Scopus (355) Google Scholar, 7Jacobsen S.E. Sakai H. Finnegan E.J. Cao X. Meyerowitz E.M. Ectopic hypermethylation of flower-specific genes in Arabidopsis.Curr. Biol. 2000; 10: 179-186Abstract Full Text Full Text PDF PubMed Scopus (205) Google Scholar, 8Kishimoto N. Sakai H. Jackson J. Jacobsen S.E. Meyerowitz E.M. Dennis E.S. Finnegan E.J. Site specificity of the Arabidopsis METI DNA methyltransferase demonstrated through hypermethylation of the superman locus.Plant Mol. Biol. 2001; 46: 171-183Crossref PubMed Scopus (64) Google Scholar, 9Lindroth A.M. Cao X. Jackson J.P. Zilberman D. McCallum C.M. Henikoff S. Jacobsen S.E. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation.Science. 2001; 292: 2077-2080Crossref PubMed Scopus (697) Google Scholar, 10Jackson J.P. Lindroth A.M. Cao X. Jacobsen S.E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase.Nature. 2002; 416: 556-560Crossref PubMed Scopus (1017) Google Scholar, 11Cao X. Jacobsen S.E. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes.Proc. Natl. Acad. Sci. USA. 2002; 99: 16491-16498Crossref PubMed Scopus (470) Google Scholar]. To understand how the SUP gene is expressed spatially and temporally in its restricted domain, and why methylation of the transcribed region affects early-stage SUP expression, we have identified the SUP cis regulatory elements by characterizing SUP gene fusions. These studies show that the SUP gene has discrete upstream promoter elements required for expression in stamen primordia in early stages and in the ovary in later stages. The promoter activity for stamen primordia is modulated by several positive and negative elements located in the transcribed and translated regions. Several regulatory elements in the transcribed region correlate with the areas of the gene that are heavily methylated in epigenetic alleles; these data provide a possible explanation of how methylation of the transcribed region represses transcription.