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SUPERMAN regulates floral whorl boundaries through control of auxin biosynthesis

Xu, Yifeng and Prunet, Nathanaël and Gan, Eng-Seng and Wang, Yanbin and Stewart, Darragh and Wellmer, Frank and Huang, Jiangbo and Yamaguchi, Norutoshi and Tatsumi, Yoshitaka and Kojima, Mikiko and Kiba, Takatoshi and Sakakibara, Hitoshi and Jack, Thomas P. and Meyerowitz, Elliot M. and Ito, Toshiro (2018) SUPERMAN regulates floral whorl boundaries through control of auxin biosynthesis. EMBO Journal, 37 (11). Art. No. e97499. ISSN 0261-4189. PMCID PMC5983216. doi:10.15252/embj.201797499. https://resolver.caltech.edu/CaltechAUTHORS:20180620-121823934

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Abstract

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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://dx.doi.org/10.15252/embj.201797499DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc5983216/PubMed CentralArticle
ORCID:
AuthorORCID
Prunet, Nathanaël0000-0002-8939-5920
Meyerowitz, Elliot M.0000-0003-4798-5153
Ito, Toshiro0000-0002-8206-2787
Additional Information:© 2018 The Authors. Received 4 June 2017 | Revised 25 March 2018 | Accepted 4 April 2018 | Published online 15 May 2018. The authors would like to thank Jing Han Hong for reading the draft of this manuscript, Shen Lisha for the BiFC and Y2H constructs for some PcG components, and Jian Xu for the pDR5rev::GFP seeds and the unpublished transgenic plants that contain the IAAH gene. This work was supported by grants from the NAIST Foundation, the Mitsubishi Foundation, Grant‐in‐Aid for Scientific Research on Innovative Areas (Nos. 17H05843), Grant‐in‐Aid for Scientific Research A (No. 15H02405), Temasek Life Sciences Laboratory (TLL), and the National Research Foundation Singapore under the Competitive Research Programme (CRP Award NRFCRP001‐108) to T.I. Funding in the Meyerowitz Laboratory was provided by the Howard Hughes Medical Institute, the US National Institutes of Health through grant R01 GM104244, and the Gordon and Betty Moore Foundation through Grant GBMF3406. Funding in the Jack laboratory was provided by the US National Science Foundation through grant IOS‐0926347. Funding in the Wellmer laboratory was provided by the Science Foundation Ireland through grant #10/IN.1/B2971. Funding: NAIST Foundation; Mitsubishi Foundation; Grant‐in‐Aid for Scientific Research 17H05843, 15H02405, 15K14549; Temasek Life Sciences Laboratory; National Research Foundation Singapore NRFCRP001‐108; US National Institutes of Health R01 GM104244; Gordon and Betty Moore Foundation GBMF3406; US National Science Foundation IOS‐0926347; Science Foundation Ireland 10/IN.1/B2971. Author contributions: YX and TI conceived the study. TI supervised and coordinated the study. YX, NP, EMM, and TI designed the experiments. YX and YW performed the Y2H, BiFC, and Co‐IP assays. YX, NP, and TI prepared all the constructs and the transgenic lines. YX and NP took the confocal images. YX and E‐SG carried out the microarray analysis and ChIP experiments. YX and NY carried out the genetic analysis. NY, YT, MK, TK, and HS quantified the auxin amount. YX and DS did transcriptional analysis. YX performed the SEM analysis. YX and JH performed the chemical treatments. YX, TI, NP, and EMM wrote the manuscript. TPJ and FW edited the manuscript. All authors discussed the results and approved the final manuscript. The authors declare that they have no conflict of interest.
Funders:
Funding AgencyGrant Number
NAIST FoundationUNSPECIFIED
Mitsubishi FoundationUNSPECIFIED
Ministry of Education, Culture, Sports, Science and Technology (MEXT)17H05843
Ministry of Education, Culture, Sports, Science and Technology (MEXT)15H02405
Ministry of Education, Culture, Sports, Science and Technology (MEXT)15K14549
Temasek Life Sciences LaboratoryUNSPECIFIED
National Research Foundation (Singapore)NRFCRP001‐108
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NIHR01 GM104244
Gordon and Betty Moore FoundationGBMF3406
NSFIOS‐0926347
Science Foundation, Ireland10/IN.1/B2971
Subject Keywords:auxin; floral meristem; floral organogenesis; H3K27me3; polycomb repressive complexes; SUPERMAN
Issue or Number:11
PubMed Central ID:PMC5983216
DOI:10.15252/embj.201797499
Record Number:CaltechAUTHORS:20180620-121823934
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180620-121823934
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:87264
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:20 Jun 2018 20:21
Last Modified:15 Nov 2021 20:46

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