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      Sugars and the speed of life—Metabolic signals that determine plant growth, development and death

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      1 , , 1
      Physiologia Plantarum
      Blackwell Publishing Ltd

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          Abstract

          Plant growth and development depend on the availability of carbohydrates synthesised in photosynthesis (source activity) and utilisation of these carbohydrates for growth (sink activity). External conditions, such as temperature, nutrient availability and stress, can affect source as well as sink activity. Optimal utilisation of resources is under circadian clock control. This molecular timekeeper ensures that growth responses are adjusted to different photoperiod and temperature settings by modulating starch accumulation and degradation accordingly. For example, during the night, starch degradation is required to provide sugars for growth. Under favourable growth conditions, high sugar availability stimulates growth and development, resulting in an overall accelerated life cycle of annual plants. Key signalling components include trehalose‐6‐phosphate (Tre6P), which reflects sucrose availability and stimulates growth and branching when the conditions are favourable. Under sink limitation, Tre6P does, however, inhibit night‐time starch degradation. Tre6P interacts with Sucrose‐non‐fermenting1‐Related Kinase1 (SnRK1), a protein kinase that inhibits growth under starvation and stress conditions and delays development (including flowering and senescence). Tre6P inhibits SnRK1 activity, but SnRK1 increases the Tre6P to sucrose ratio under favourable conditions. Alongside Tre6P, Target of Rapamycin (TOR) stimulates processes such as protein synthesis and growth when sugar availability is high. In annual plants, an accelerated life cycle results in early leaf and plant senescence, thus shortening the lifespan. While the availability of carbohydrates in the form of sucrose and other sugars also plays an important role in seasonal life cycle events (phenology) of perennial plants, the sugar signalling pathways in perennials are less well understood.

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          The worldwide leaf economics spectrum.

          Bringing together leaf trait data spanning 2,548 species and 175 sites we describe, for the first time at global scale, a universal spectrum of leaf economics consisting of key chemical, structural and physiological properties. The spectrum runs from quick to slow return on investments of nutrients and dry mass in leaves, and operates largely independently of growth form, plant functional type or biome. Categories along the spectrum would, in general, describe leaf economic variation at the global scale better than plant functional types, because functional types overlap substantially in their leaf traits. Overall, modulation of leaf traits and trait relationships by climate is surprisingly modest, although some striking and significant patterns can be seen. Reliable quantification of the leaf economics spectrum and its interaction with climate will prove valuable for modelling nutrient fluxes and vegetation boundaries under changing land-use and climate.
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            Glc-TOR signalling leads transcriptome reprogramming and meristem activation

            Meristems encompass stem/progenitor cells that sustain postembryonic growth of all plant organs. How meristems are activated and sustained by nutrient signalling remains enigmatic in photosynthetic plants. Combining chemical manipulations and chemical genetics at the photoautotrophic transition checkpoint, we reveal that shoot photosynthesis-derived glucose drives target-of-rapamycin (TOR) signalling relays through glycolysis and mitochondrial bioenergetics to control root meristem activation, which is decoupled from direct glucose sensing, growth-hormone signalling, and stem-cell maintenance. Surprisingly, glucose-TOR signalling dictates transcriptional reprogramming of remarkable gene sets involved in central and secondary metabolism, cell cycle, transcription, signalling, transport and folding. Systems, cellular and genetic analyses uncover TOR phosphorylation of E2Fa transcription factor for an unconventional activation of S-phase genes, and glucose-signalling defects in e2fa root meristems. Our findings establish pivotal roles of glucose-TOR signalling in unprecedented transcriptional networks wiring central metabolism and biosynthesis for energy and biomass production, and integrating localized stem/progenitor-cell proliferation through inter-organ nutrient coordination to control developmental transition and growth.
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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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                Author and article information

                Contributors
                astrid.wingler@ucc.ie
                Journal
                Physiol Plant
                Physiol Plant
                10.1111/(ISSN)1399-3054
                PPL
                Physiologia Plantarum
                Blackwell Publishing Ltd (Oxford, UK )
                0031-9317
                1399-3054
                14 March 2022
                Mar-Apr 2022
                : 174
                : 2 ( doiID: 10.1111/ppl.v174.2 )
                : e13656
                Affiliations
                [ 1 ] School of Biological, Earth & Environmental Sciences and Environmental Research Institute University College Cork, Distillery Fields Cork
                Author notes
                [*] [* ] Correspondence

                Astrid Wingler, School of Biological, Earth & Environmental Sciences and Environmental Research Institute, University College Cork, Distillery Fields, North Mall, Cork T23 TK30.

                Email: astrid.wingler@ 123456ucc.ie

                Author information
                https://orcid.org/0000-0003-4229-2497
                https://orcid.org/0000-0002-9394-0098
                Article
                PPL13656
                10.1111/ppl.13656
                9314607
                35243645
                295e790c-3f8c-46b0-a0fa-fcf806941b45
                © 2022 The Authors. Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 24 February 2022
                : 31 December 2021
                : 01 March 2022
                Page count
                Figures: 2, Tables: 0, Pages: 10, Words: 11082
                Categories
                Biochemistry and Metabolism
                Special Issue Article
                Special Issue Articles
                Custom metadata
                2.0
                March/April 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.7 mode:remove_FC converted:26.07.2022

                Plant science & Botany
                Plant science & Botany

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