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      APETALA2 antagonizes the transcriptional activity of AGAMOUS in regulating floral stem cells in Arabidopsis thaliana

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          Summary

          • APETALA2 ( AP2 ) is best known for its function in the outer two floral whorls, where it specifies the identities of sepals and petals by restricting the expression of AGAMOUS ( AG ) to the inner two whorls in Arabidopsis thaliana. Here, we describe a role of AP2 in promoting the maintenance of floral stem cell fate, not by repressing AG transcription, but by antagonizing AG activity in the center of the flower.

          • We performed a genetic screen with ag‐10 plants, which exhibit a weak floral determinacy defect, and isolated a mutant with a strong floral determinacy defect. This mutant was found to harbor another mutation in AG and was named ag‐11. We performed a genetic screen in the ag‐11 background to isolate mutations that suppress the floral determinacy defect. Two suppressor mutants were found to harbor mutations in AP2 .

          • While AG is known to shut down the expression of the stem cell maintenance gene WUSCHEL ( WUS ) to terminate floral stem cell fate, AP2 promotes the expression of WUS .

          • AP2 does not repress the transcription of AG in the inner two whorls, but instead counteracts AG activity.

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          Most cited references36

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          A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development.

          X. Chen (2004)
          Plant microRNAs (miRNAs) show a high degree of sequence complementarity to, and are believed to guide the cleavage of, their target messenger RNAs. Here, I show that miRNA172, which can base-pair with the messenger RNA of a floral homeotic gene, APETALA2, regulates APETALA2 expression primarily through translational inhibition. Elevated miRNA172 accumulation results in floral organ identity defects similar to those in loss-of-function apetala2 mutants. Elevated levels of mutant APETALA2 RNA with disrupted miRNA172 base pairing, but not wild-type APETALA2 RNA, result in elevated levels of APETALA2 protein and severe floral patterning defects. Therefore, miRNA172 likely acts in cell-fate specification as a translational repressor of APETALA2 in Arabidopsis flower development.
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            The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes.

            The higher-plant shoot meristem is a dynamic structure whose maintenance depends on the coordination of two antagonistic processes, organ initiation and self-renewal of the stem cell population. In Arabidopsis shoot and floral meristems, the WUSCHEL (WUS) gene is required for stem cell identity, whereas the CLAVATA1, 2, and 3 (CLV) genes promote organ initiation. Our analysis of the interactions between these key regulators indicates that (1) the CLV genes repress WUS at the transcript level and that (2) WUS expression is sufficient to induce meristem cell identity and the expression of the stem cell marker CLV3. Our data suggest that the shoot meristem has properties of a self-regulatory system in which WUS/CLV interactions establish a feedback loop between the stem cells and the underlying organizing center.
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              The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors.

              Mutations in the homeotic gene agamous of the plant Arabidopsis cause the transformation of the floral sex organs. Cloning and sequence analysis of agamous suggest that it encodes a protein with a high degree of sequence similarity to the DNA-binding region of transcription factors from yeast and humans and to the product of a homeotic gene from Antirrhinum. The agamous gene therefore probably encodes a transcription factor that regulates genes determining stamen and carpel development in wild-type flowers.
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                Author and article information

                Contributors
                langtaoxiao@163.com
                xuemei.chen@ucr.edu
                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                08 September 2016
                August 2017
                : 215
                : 3 ( doiID: 10.1111/nph.2017.215.issue-3 )
                : 1197-1209
                Affiliations
                [ 1 ] Hunan Provincial Key Laboratory of Phytohormones and Growth Development Hunan Provincial Key Laboratory for Crop Germplasm Innovation and Utilization Hunan Agricultural University Changsha 410128 China
                [ 2 ] Department of Botany and Plant Sciences Institute of Integrative Genome Biology University of California Riverside CA 92521 USA
                [ 3 ] College of Horticulture Nanjing Agricultural University No. 1 Weigang Nanjing 210095 China
                [ 4 ] State Key Laboratory of Genetic Engineering Collaborative Innovation Center for Genetics and Development Institute of Plant Biology School of Life Sciences Fudan University Shanghai 200438 China
                [ 5 ] State Key Laboratory of Plant Cell and Chromosome Engineering Center for Agricultural Resources Research Institute of Genetics and Developmental Biology Chinese Academy of Sciences Shijiazhuang 050021 China
                [ 6 ] Guangdong Provincial Key Laboratory for Plant Epigenetics College of Life Sciences and Oceanography Shenzhen University Shenzhen 518060 China
                [ 7 ] Howard Hughes Medical Institute University of California Riverside CA 92521 USA
                Author notes
                [*] [* ] Authors for correspondence:

                Xuemei Chen

                Tel: +1 951 827 3988

                Email: xuemei.chen@ 123456ucr.edu

                Langtao Xiao

                Tel: +86 731 8463 5261

                Email: langtaoxiao@ 123456163.com

                [†]

                These authors contributed equally to this work.

                Article
                NPH14151 2016-22273
                10.1111/nph.14151
                5342953
                27604611
                4b8e4d66-f309-4d1e-9ff0-b6db4128ddcd
                © 2016 The Authors. New Phytologist © 2016 New Phytologist Trust

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 June 2016
                : 18 July 2016
                Page count
                Figures: 7, Tables: 0, Pages: 13, Words: 9015
                Funding
                Funded by: National Institutes of Health
                Award ID: GM061146
                Funded by: National Natural Science Foundation of China
                Award ID: 31570372
                Funded by: China Scholarship Council
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph14151
                August 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.1.4 mode:remove_FC converted:19.07.2017

                Plant science & Botany
                agamous,apetala2,floral determinacy,floral stem cells,knuckles,wuschel
                Plant science & Botany
                agamous, apetala2, floral determinacy, floral stem cells, knuckles, wuschel

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