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Open Access Research article

FILAMENTOUS FLOWER controls lateral organ development by acting as both an activator and a repressor

Oliver Bonaccorso1, Joanne E Lee1, Libby Puah1, Charles P Scutt2 and John F Golz1*

Author Affiliations

1 Department of Genetics, University of Melbourne, Royal Parade, Parkville, VIC 3010, Australia

2 Laboratoire de Reproduction et Développement des Plantes, UMR 5667- CNRS/INRA/Université de Lyon, École Normale Supérieure de Lyon, 46, allée d'Italie 69364, Lyon Cedex, 07, France

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BMC Plant Biology 2012, 12:176  doi:10.1186/1471-2229-12-176

Published: 1 October 2012

Abstract

Background

The YABBY (YAB) family of transcription factors participate in a diverse range of processes that include leaf and floral patterning, organ growth, and the control of shoot apical meristem organisation and activity. How these disparate functions are regulated is not clear, but based on interactions with the LEUNIG-class of co-repressors, it has been proposed that YABs act as transcriptional repressors. In the light of recent work showing that DNA-binding proteins associated with the yeast co-repressor TUP1 can also function as activators, we have examined the transcriptional activity of the YABs.

Results

Of the four Arabidopsis YABs tested in yeast, only FILAMENTOUS FLOWER (FIL) activated reporter gene expression. Similar analysis with Antirrhinum YABs identified the FIL ortholog GRAMINIFOLIA as an activator. Plant-based transactivation assays not only confirmed the potential of FIL to activate transcription, but also extended this property to the FIL paralog YABBY3 (YAB3). Subsequent transcriptomic analysis of lines expressing a steroid-inducible FIL protein revealed groups of genes that responded either positively or negatively to YAB induction. Included in the positively regulated group of genes were the polarity regulators KANADI1 (KAN1), AUXIN RESPONSE FACTOR 4 (ARF4) and ASYMMETRIC LEAVES1 (AS1). We also show that modifying FIL to function as an obligate repressor causes strong yab loss-of-function phenotypes.

Conclusions

Collectively these data show that FIL functions as a transcriptional activator in plants and that this activity is involved in leaf patterning. Interestingly, our study also supports the idea that FIL can act as a repressor, as transcriptomic analysis identified negatively regulated FIL-response genes. To reconcile these observations, we propose that YABs are bifunctional transcription factors that participate in both positive and negative regulation. These findings fit a model of leaf development in which adaxial/abaxial patterning is maintained by a regulatory network consisting of positive feedback loops.

Keywords:
YABBYs; Arabidopsis thaliana; Leaf patterning and development; Adaxial-abaxial polarity; Lateral organ formation