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

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.

SUBMITTER: Bonaccorso O

PROVIDER: S-EPMC3520853 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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

Bonaccorso Oliver O Lee Joanne E JE Puah Libby L Scutt Charles P CP Golz John F JF

BMC plant biology 20121001

<h4>Background</h4>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 wit ...[more]

PMID: 23025792

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Project description:Plant inflorescence meristems and floral meristems possess specific boundary domains that result in floral organ separation, and in proper numbers of floral organs. HANABA TARANU (HAN) encodes a boundary-expressing GATA type zinc finger transcription factor that regulates shoot apical meristem organization, cell division and flower development in Arabidopsis, but the underlying mechanism remains unclear. Through time-course whole genome oligonucleotide microarray analyses following transient overexpression of HAN, we find that HAN represses hundreds of genes, especially genes involved in hormone responses and floral organ regulation. Transient overexpression of HAN also causes the repression of HAN itself and three other HAN family genes: HANL2 (HAN-LIKE2), GNC (GATA, NITRATE-INDUCIBLE, CARBON-METABOLISM-INVOLVED) and GNL (GNC LIKE), forming a negative regulatory feedback loop. Double- and triple-mutant strains of han with hanl2, gnc and gnl show synergistic effects on sepal fusion, petal number, and silique length, and embryo development, as well as carpelloid stamens. Transcripts of HANL2, GNC and GNL have similar accumulation patterns, specifically in petals, stamens, carpels and inflorescence meristems, which are partially overlapping with the expression pattern of HAN, suggesting that HAN and HAN family genes share redundant functions during flower development. We further show by yeast two hybrid assays that HAN can homodimerize as well as heterodimerize with other HAN family proteins. Chromatin-immunoprecipitation analyses indicate that HAN directly binds to its own promoter and the promoter of GNC in vivo. These findings, together with the fact that constitutive overexpression of HAN has an even stronger phenotype than a loss of function mutation, support the hypothesis that HAN may function as a key repressor that regulates floral development via intricate regulatory networks involving genes in the GATA3 family, hormone actions and floral organ specification.

Dataset Information

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

Publications

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

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