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Repression of AGAMOUS by BELLRINGER in Floral and Inflorescence Meristems

^a Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742
^b Department of Genetics, North Carolina State University, Raleigh, North Carolina 27695
^c Celera Genomics, Rockville, Maryland 20850

¹ To whom correspondence should be addressed. E-mail zl17{at}umail.umd.edu; fax 301-314-9082.

A common aspect of gene regulation in all developmental systems is the sustained repression of key regulatory genes in inappropriate spatial or temporal domains. To understand the mechanism of transcriptional repression of the floral homeotic gene AGAMOUS (AG), we identified two mutations in the BELLRINGER (BLR) gene based on a striking floral phenotype, in which homeotic transformations from sepals to carpels are found in flowers derived from old terminating shoots. Furthermore, this phenotype is drastically enhanced by growth at a high temperature and by combining blr with mutants of LEUNIG and SEUSS, two putative transcriptional corepressors of AG. We showed that the floral phenotype of blr mutants is caused by derepression of AG, suggesting that BLR functions as a transcription repressor. Because BLR encodes a BELL1-like (BELL) homeobox protein, direct binding of BLR to AG cis-regulatory elements was tested by gel-shift assays, and putative BLR binding motifs were identified. In addition, these putative BLR binding motifs were shown to be conserved in 17 of the 29 Brassicaceae species by phylogenetic footprinting. Because BELL homeobox proteins are a family of plant-specific transcription factors with 12 members in Arabidopsis thaliana, our findings will facilitate the identification of regulatory targets of other BELL proteins and help determine their biological functions. The age-dependent and high temperature–enhanced derepression of AG in blr mutants led us to propose that AG expression might be regulated by a thermal time-dependent molecular mechanism.

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