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      Chromatin-mediated feed-forward auxin biosynthesis in floral meristem determinacy

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          Abstract

          In flowering plants, the switch from floral stem cell maintenance to gynoecium (female structure) formation is a critical developmental transition for reproductive success. In Arabidopsis thaliana, AGAMOUS (AG) terminates floral stem cell activities to trigger this transition. Although CRABS CLAW ( CRC) is a direct target of AG, previous research has not identified any common targets. Here, we identify an auxin synthesis gene, YUCCA4 ( YUC4) as a common direct target. Ectopic YUC4 expression partially rescues the indeterminate phenotype and cell wall defects that are caused by the crc mutation. The feed-forward YUC4 activation by AG and CRC directs a precise change in chromatin state for the shift from floral stem cell maintenance to gynoecium formation. We also showed that two auxin-related direct CRC targets, YUC4 and TORNADO2, cooperatively contribute to the termination of floral stem cell maintenance. This finding provides new insight into the CRC-mediated auxin homeostasis regulation for proper gynoecium formation.

          Abstract

          In Arabidopsis, the AG and CRC transcription factors terminate floral stem cells and allow the emergence of female floral organs. Here the authors show that AG and CRC form a feed-forward loop that controls local auxin biosynthesis via induction of YUCCA4 to ensure successful gynoecium formation.

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          Most cited references63

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          The biology of chromatin remodeling complexes.

          The packaging of chromosomal DNA by nucleosomes condenses and organizes the genome, but occludes many regulatory DNA elements. However, this constraint also allows nucleosomes and other chromatin components to actively participate in the regulation of transcription, chromosome segregation, DNA replication, and DNA repair. To enable dynamic access to packaged DNA and to tailor nucleosome composition in chromosomal regions, cells have evolved a set of specialized chromatin remodeling complexes (remodelers). Remodelers use the energy of ATP hydrolysis to move, destabilize, eject, or restructure nucleosomes. Here, we address many aspects of remodeler biology: their targeting, mechanism, regulation, shared and unique properties, and specialization for particular biological processes. We also address roles for remodelers in development, cancer, and human syndromes.
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            TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.

            Plants have evolved a tremendous ability to respond to environmental changes by adapting their growth and development. The interaction between hormonal and developmental signals is a critical mechanism in the generation of this enormous plasticity. A good example is the response to the hormone ethylene that depends on tissue type, developmental stage, and environmental conditions. By characterizing the Arabidopsis wei8 mutant, we have found that a small family of genes mediates tissue-specific responses to ethylene. Biochemical studies revealed that WEI8 encodes a long-anticipated tryptophan aminotransferase, TAA1, in the essential, yet genetically uncharacterized, indole-3-pyruvic acid (IPA) branch of the auxin biosynthetic pathway. Analysis of TAA1 and its paralogues revealed a link between local auxin production, tissue-specific ethylene effects, and organ development. Thus, the IPA route of auxin production is key to generating robust auxin gradients in response to environmental and developmental cues.
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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
                itot@bs.naist.jp
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                11 December 2018
                11 December 2018
                2018
                : 9
                : 5290
                Affiliations
                [1 ]ISNI 0000 0000 9227 2257, GRID grid.260493.a, Division of Biological Science, Graduate School of Science and Technology, , Nara Institute of Science and Technology, ; 8916-5, Takayama, Ikoma, Nara 630-0192 Japan
                [2 ]ISNI 0000 0004 1754 9200, GRID grid.419082.6, Precursory Research for Embryonic Science and Technology, , Japan Science and Technology Agency, ; 4-1-8, Honcho, Kawaguchi-shi, Saitama 332-0012 Japan
                [3 ]ISNI 0000 0001 2180 6431, GRID grid.4280.e, Temasek Life Sciences Laboratory, 1 Research Link, , National University of Singapore, ; Singapore, 117604 Republic of Singapore
                [4 ]ISNI 0000 0000 8863 9909, GRID grid.262576.2, Ritsumeikan Global Innovation Research Organization, , Ritsumeikan University, ; 1-1-1, Shiga, 525-8577 Japan
                [5 ]ISNI 0000000094465255, GRID grid.7597.c, RIKEN Center for Sustainable Resource Science, ; 1-7-22, Suehiro, Tsurumi, Yokohama 230-0045 Japan
                [6 ]ISNI 0000 0001 0943 978X, GRID grid.27476.30, Department of Applied Biosciences, Graduate School of Bioagricultural Sciences, , Nagoya University, ; Chikusa, Nagoya 464-8601 Japan
                [7 ]ISNI 0000 0001 2248 6943, GRID grid.69566.3a, Graduate School of Life Sciences, , Tohoku University, ; Aoba-ku, Sendai 980-8578 Japan
                Author information
                http://orcid.org/0000-0003-3738-6157
                http://orcid.org/0000-0001-9986-2839
                http://orcid.org/0000-0001-8651-0404
                http://orcid.org/0000-0002-0073-9564
                Article
                7763
                10.1038/s41467-018-07763-0
                6289996
                30538233
                6fc6f171-e20f-4a03-b74c-d3d91f30931f
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 14 June 2018
                : 20 November 2018
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