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      Overexpression of Prunus DAM6 inhibits growth, represses bud break competency of dormant buds and delays bud outgrowth in apple plants

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          Abstract

          Most deciduous fruit trees cultivated in the temperate zone require a genotype-dependent amounts of chilling exposure for dormancy release and bud break. In Japanese apricot ( Prunus mume), DORMANCY-ASSOCIATED MADS-box 6 ( PmDAM6) may influence chilling-mediated dormancy release and bud break. In this study, we attempted to elucidate the biological functions of PmDAM6 related to dormancy regulation by analyzing PmDAM6-overexpressing transgenic apple ( Malus spp.). We generated 35S: PmDAM6 lines and chemically inducible overexpression lines, 35S: PmDAM6-GR. In both overexpression lines, shoot growth was inhibited and early bud set was observed. In addition, PmDAM6 expression repressed bud break competency during dormancy and delayed bud break. Moreover, PmDAM6 expression increased abscisic acid levels and decreased cytokinins contents during the late dormancy and bud break stages in both 35S: PmDAM6 and 35S: PmDAM6-GR. Our analysis also suggested that abscisic acid levels increased during dormancy but subsequently decreased during dormancy release whereas cytokinins contents increased during the bud break stage in dormant Japanese apricot buds. We previously revealed that PmDAM6 expression is continuously down-regulated during dormancy release toward bud break in Japanese apricot. The PmDAM6 expression pattern was concurrent with a decrease and increase in the abscisic acid and cytokinins contents, respectively, in dormant Japanese apricot buds. Therefore, we hypothesize that PmDAM6 represses the bud break competency during dormancy and bud break stages in Japanese apricot by modulating abscisic acid and cytokinins accumulation in dormant buds.

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          The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms.

          In tree species native to temperate and boreal regions, the activity-dormancy cycle is an important adaptive trait both for survival and growth. We discuss recent research on mechanisms controlling the overlapping developmental processes that define the activity-dormancy cycle, including cessation of apical growth, bud development, induction, maintenance and release of dormancy, and bud burst. The cycle involves an extensive reconfiguration of metabolism. Environmental control of the activity-dormancy cycle is based on perception of photoperiodic and temperature signals, reflecting adaptation to prevailing climatic conditions. Several molecular actors for control of growth cessation have been identified, with the CO/FT regulatory network and circadian clock having important coordinating roles in control of growth and dormancy. Other candidate regulators of bud set, dormancy and bud burst have been identified, such as dormancy-associated MADS-box factors, but their exact roles remain to be discovered. Epigenetic mechanisms also appear to factor in control of the activity-dormancy cycle. Despite evidence for gibberellins as negative regulators in growth cessation, and ABA and ethylene in bud formation, understanding of the roles that plant growth regulators play in controlling the activity-dormancy cycle is still very fragmentary. Finally, some of the challenges for further research in bud dormancy are discussed. © 2012 Blackwell Publishing Ltd.
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            A glucocorticoid-mediated transcriptional induction system in transgenic plants.

            A novel chemical induction system for transcription in plants has been developed, taking advantage of the regulatory mechanism of vertebrate steroid hormone receptors. A chimeric transcription of the DNA-binding domain of the yeast transcription factor GAL4, the transactivating domain of the herpes viral protein VP16, and the receptor domain of the rat glucocorticoid receptor (GR). The GVG gene was introduced into transgenic tobacco and Arabidopsis together with a luciferase (Luc) gene which was transcribed from a promoter containing six tandem copies of the GAL4 upstream activating sequence. Induction of luciferase activity was observed when the transgenic tobacco plants were grown on an agar medium containing dexamethasone (DEX), a strong synthetic glucocorticoid. Induction levels of the luciferase activity were well correlated with DEX concentrations in the range from 0.1 to 10 microM and the maximum expression level was over 100 times that of the basal level. Analysis of the induction kinetics by Northern blot analysis showed that the Luc mRNA was first detected 1 h after DEX treatment and increased to the maximum level in 4 h. The stationary induction level and the duration of the induction varied with the glucocorticoid derivative used. The GVG gene activity can also be regulated by DEX in transgenic Arabidopsis plants. The results indicate that a stringent chemical control of transcription can be achieved in plants with the GVG system. Advantages and potential uses of this system are also discussed.
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              A molecular timetable for apical bud formation and dormancy induction in poplar.

              The growth of perennial plants in the temperate zone alternates with periods of dormancy that are typically initiated during bud development in autumn. In a systems biology approach to unravel the underlying molecular program of apical bud development in poplar (Populus tremula x Populus alba), combined transcript and metabolite profiling were applied to a high-resolution time course from short-day induction to complete dormancy. Metabolite and gene expression dynamics were used to reconstruct the temporal sequence of events during bud development. Importantly, bud development could be dissected into bud formation, acclimation to dehydration and cold, and dormancy. To each of these processes, specific sets of regulatory and marker genes and metabolites are associated and provide a reference frame for future functional studies. Light, ethylene, and abscisic acid signal transduction pathways consecutively control bud development by setting, modifying, or terminating these processes. Ethylene signal transduction is positioned temporally between light and abscisic acid signals and is putatively activated by transiently low hexose pools. The timing and place of cell proliferation arrest (related to dormancy) and of the accumulation of storage compounds (related to acclimation processes) were established within the bud by electron microscopy. Finally, the identification of a large set of genes commonly expressed during the growth-to-dormancy transitions in poplar apical buds, cambium, or Arabidopsis thaliana seeds suggests parallels in the underlying molecular mechanisms in different plant organs.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – original draftRole: Writing – review & editing
                Role: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Methodology
                Role: Data curationRole: Formal analysisRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Methodology
                Role: Investigation
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Investigation
                Role: Validation
                Role: MethodologyRole: Project administrationRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                9 April 2019
                2019
                : 14
                : 4
                : e0214788
                Affiliations
                [1 ] Laboratory of Pomology, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
                [2 ] Division of Apple Research, Institute of Fruit Tree and Tea Science, NARO, Morioka, Japan
                [3 ] Institute of Plant Science and Resources, Okayama University, Kurashiki, Japan
                [4 ] Agricultural Experimental Station, Ishikawa Prefectural University, Nonoichi, Japan
                [5 ] RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama, Japan
                Purdue University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                [¤a]

                Current address: Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan

                [¤b]

                Current address: Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan

                Author information
                http://orcid.org/0000-0002-9044-7863
                Article
                PONE-D-18-18508
                10.1371/journal.pone.0214788
                6456227
                30964897
                c2316c57-555c-4f50-b13e-91155f2a6e5d
                © 2019 Yamane et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 June 2018
                : 20 March 2019
                Page count
                Figures: 8, Tables: 2, Pages: 24
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: KAKENHI 23380017
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: KAKENHI 26252005
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: KAKENHI 18H02198
                Award Recipient :
                This study was supported by the Japan Society for the Promotion of Science (Grant-in-Aids KAKENHI Nos. 23380017, 26252005, 18H02198) to HY. https://www.jsps.go.jp/english/index.html. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Biology and Life Sciences
                Plant Science
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