SUPERMAN regulates floral whorl boundaries through control of auxin biosynthesis

• Published in: The EMBO journal Vol. 37; no. 11
• Main Authors: Xu, Yifeng, Prunet, Nathanaël, Gan, Eng‐Seng, Wang, Yanbin, Stewart, Darragh, Wellmer, Frank, Huang, Jiangbo, Yamaguchi, Nobutoshi, Tatsumi, Yoshitaka, Kojima, Mikiko, Kiba, Takatoshi, Sakakibara, Hitoshi, Jack, Thomas P, Meyerowitz, Elliot M, Ito, Toshiro
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.06.2018; Blackwell Publishing Ltd; John Wiley and Sons Inc
• Subjects: Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; auxin; Biosynthesis; Carpels; Derepression; EMBO30; floral meristem; floral organogenesis; Flowers; Flowers - genetics; Flowers - growth & development; Gene expression; Gene Expression Regulation, Plant; Genes; H3K27me3; Indoleacetic Acids - metabolism; Meristem - genetics; Meristems; Mixed Function Oxygenases - genetics; Mutation; Organogenesis; Organogenesis, Plant - genetics; Organs; Phenotype; Plant hormones; Plant reproductive structures; Plant species; Polycomb group proteins; Polycomb Repressive Complex 2 - genetics; polycomb repressive complexes; Regulatory mechanisms (biology); Reproductive organs; Signal transduction; Signaling; Stamens; Stem cells; Stem Cells - metabolism; SUPERMAN; Supernumerary; Transcription Factors - genetics; floral meristem; auxin; polycomb repressive complexes; floral organogenesis; SUPERMAN; H3K27me3
• DOI: 10.15252/embj.201797499
• ISSN: 0261-4189

Proper floral patterning, including the number and position of floral organs in most plant species, is tightly controlled by the precise regulation of the persistence and size of floral meristems (FMs). In Arabidopsis , two known feedback pathways, one composed of WUSCHEL (WUS) and CLAVATA3 (CLV3) and the other composed of AGAMOUS (AG) and WUS, spatially and temporally control floral stem cells, respectively. However, mounting evidence suggests that other factors, including phytohormones, are also involved in floral meristem regulation. Here, we show that the boundary gene SUPERMAN ( SUP ) bridges floral organogenesis and floral meristem determinacy in another pathway that involves auxin signaling. SUP interacts with components of polycomb repressive complex 2 (PRC2) and fine‐tunes local auxin signaling by negatively regulating the expression of the auxin biosynthesis genes YUCCA1/4 ( YUC1/4 ). In sup mutants, derepressed local YUC1/4 activity elevates auxin levels at the boundary between whorls 3 and 4, which leads to an increase in the number and the prolonged maintenance of floral stem cells, and consequently an increase in the number of reproductive organs. Our work presents a new floral meristem regulatory mechanism, in which SUP , a boundary gene, coordinates floral organogenesis and floral meristem size through fine‐tuning auxin biosynthesis. Synopsis SUPERMAN (SUP) controls the specification and maintenance of the boundary between stamens in whorl 3 and carpels in whorl 4. This boundary gene functions as an active repressor of auxin biosynthesis that regulates flower development, the absence of which leads to flowers with supernumerary stamens. SUP recruits the Polycomb Group (PcG) component CURLY LEAF (CLF) to directly repress auxin biosynthesis genes YUCCA1 and 4 (YUC1/4) locally. The derepression of YUC1/4 in sup mutants causes ectopic auxin activity at the whorl 3/4 boundary region. Perturbed auxin activity in sup flowers results in delayed termination of stem cell activity and increase in FM size, which then leads to increased stamen number. Graphical Abstract Transcription of auxin biosynthesis genes is repressed by the boundary gene SUPERMAN, whose absence leads to supernumerary stamen formation in Arabidopsis flowers.