Abstract
BackgroundThe 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.ResultsOf 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.ConclusionsCollectively 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.
Highlights
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
Similar observations have been made in Antirrhinum, where mutations in the FIL/YAB3 ortholog, GRAM, are associated with a loss of abaxial cell identity, whereas when combined with mutations in the YAB5 ortholog, PROLONGATA (PROL), they result in a loss of adaxial cell identity [10]
To determine whether activation is a conserved feature of the FIL subgroup of YABs, we examined whether the Antirrhinum FIL ortholog, GRAM, behaves as an activator in AD) produced a 3.3 fold increase in luciferase activity
Summary
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. Characterisation of the vegetative YABs through mutant and gain-of-function analyses has shown that they regulate cell identity in developing organs and play an important role in establishing organ polarity and subsequent lamina growth [1,2,4,6,9] This regulation is complex, as loss of FIL and YAB3 activities is associated with the partial adaxialisation of organs [2], whereas combined loss of FIL, YAB3 and YAB5 results in organ abaxialisation [4]. The precise position of YABs within these networks is not certain, but based on yab loss-of-function phenotypes it has been proposed that YABs integrate adaxialabaxial patterning with a program of lamina growth [6]
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