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      Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme

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          Abstract

          Abscisic acid (ABA) regulates abiotic stress and developmental responses including regulation of seed dormancy to prevent seeds from germinating under unfavorable environmental conditions. ABA HYPERSENSITIVE GERMINATION1 ( AHG1) encoding a type 2C protein phosphatase (PP2C) is a central negative regulator of ABA response in germination; however, the molecular function and regulation of AHG1 remain elusive. Here we report that AHG1 interacts with DELAY OF GERMINATION1 (DOG1), which is a pivotal positive regulator in seed dormancy. DOG1 acts upstream of AHG1 and impairs the PP2C activity of AHG1 in vitro. Furthermore, DOG1 has the ability to bind heme. Binding of DOG1 to AHG1 and heme are independent processes, but both are essential for DOG1 function in vivo. Our study demonstrates that AHG1 and DOG1 constitute an important regulatory system for seed dormancy and germination by integrating multiple environmental signals, in parallel with the PYL/RCAR ABA receptor-mediated regulatory system.

          Abstract

          The hormone abscisic acid (ABA) prevents seeds from germination when conditions are not suitable. Here the authors show that DOG1, a positive regulator of germination, impairs ABA signaling via genetic and physical interactions with the AHG1 phosphatase and that DOG1 binding to heme is required for this activity.

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          Most cited references55

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          Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins.

          Type 2C protein phosphatases (PP2Cs) are vitally involved in abscisic acid (ABA) signaling. Here, we show that a synthetic growth inhibitor called pyrabactin functions as a selective ABA agonist. Pyrabactin acts through PYRABACTIN RESISTANCE 1 (PYR1), the founding member of a family of START proteins called PYR/PYLs, which are necessary for both pyrabactin and ABA signaling in vivo. We show that ABA binds to PYR1, which in turn binds to and inhibits PP2Cs. We conclude that PYR/PYLs are ABA receptors functioning at the apex of a negative regulatory pathway that controls ABA signaling by inhibiting PP2Cs. Our results illustrate the power of the chemical genetic approach for sidestepping genetic redundancy.
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            Regulators of PP2C phosphatase activity function as abscisic acid sensors.

            The plant hormone abscisic acid (ABA) acts as a developmental signal and as an integrator of environmental cues such as drought and cold. Key players in ABA signal transduction include the type 2C protein phosphatases (PP2Cs) ABI1 and ABI2, which act by negatively regulating ABA responses. In this study, we identify interactors of ABI1 and ABI2 which we have named regulatory components of ABA receptor (RCARs). In Arabidopsis, RCARs belong to a family with 14 members that share structural similarity with class 10 pathogen-related proteins. RCAR1 was shown to bind ABA, to mediate ABA-dependent inactivation of ABI1 or ABI2 in vitro, and to antagonize PP2C action in planta. Other RCARs also mediated ABA-dependent regulation of ABI1 and ABI2, consistent with a combinatorial assembly of receptor complexes.
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              Abscisic Acid synthesis and response.

              Abscisic acid (ABA) is one of the "classical" plant hormones, i.e. discovered at least 50 years ago, that regulates many aspects of plant growth and development. This chapter reviews our current understanding of ABA synthesis, metabolism, transport, and signal transduction, emphasizing knowledge gained from studies of Arabidopsis. A combination of genetic, molecular and biochemical studies has identified nearly all of the enzymes involved in ABA metabolism, almost 200 loci regulating ABA response, and thousands of genes regulated by ABA in various contexts. Some of these regulators are implicated in cross-talk with other developmental, environmental or hormonal signals. Specific details of the ABA signaling mechanisms vary among tissues or developmental stages; these are discussed in the context of ABA effects on seed maturation, germination, seedling growth, vegetative stress responses, stomatal regulation, pathogen response, flowering, and senescence.
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                Author and article information

                Contributors
                nonishi@affrc.go.jp
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                6 June 2018
                6 June 2018
                2018
                : 9
                : 2132
                Affiliations
                [1 ]ISNI 0000 0001 2222 0432, GRID grid.416835.d, Radiation Breeding Division, Institute of Crop Science, , National Agriculture and Food Research Organization, ; 2425 Kamimurata, Hitachiohmiya, Ibaraki 319-2293 Japan
                [2 ]ISNI 0000 0001 2222 0432, GRID grid.416835.d, Structural Biology Team, Advanced Analysis Center, , National Agriculture and Food Research Organization, ; Tsukuba, Ibaraki 305-8602 Japan
                [3 ]ISNI 0000000122199231, GRID grid.214007.0, Department of Molecular Medicine, , The Scripps Research Institute, ; 10550 North Torrey Pines Road, La Jolla, CA 92037 USA
                [4 ]ISNI 0000 0001 0943 978X, GRID grid.27476.30, Division of Biological Science, Graduate School of Science, , Nagoya University, ; Nagoya, 464-8602 Japan
                [5 ]ISNI 0000 0001 0943 978X, GRID grid.27476.30, Institute of Transformative Bio-Molecules (WPI-ITbM), , Nagoya University, ; Chikusa, Nagoya 464-8602 Japan
                [6 ]ISNI 0000 0001 2107 4242, GRID grid.266100.3, Division of Biological Sciences, Cell and Developmental Biology Section, , University of California, San Diego, ; 9500 Gilman Drive, La Jolla, CA 92093-0116 USA
                [7 ]ISNI 0000 0001 1302 4472, GRID grid.261356.5, Institute of Plant Science and Resources, , Okayama University, ; 2-20-1 Chuo, Kurashiki, Okayama 710-0046 Japan
                [8 ]ISNI 0000 0001 2222 0432, GRID grid.416835.d, Present Address: Division of Basic Research, Institute of Crop Science, , National Agriculture and Food Research Organization, ; 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8518 Japan
                Author information
                http://orcid.org/0000-0001-5267-1672
                http://orcid.org/0000-0002-3868-2380
                Article
                4437
                10.1038/s41467-018-04437-9
                5989226
                29875377
                5f6c3ada-62c6-4804-b088-2bb994440e4e
                © 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
                : 9 September 2016
                : 1 May 2018
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