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      Integration of light and metabolic signals for stem cell activation at the shoot apical meristem

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          Abstract

          A major feature of embryogenesis is the specification of stem cell systems, but in contrast to the situation in most animals, plant stem cells remain quiescent until the postembryonic phase of development. Here, we dissect how light and metabolic signals are integrated to overcome stem cell dormancy at the shoot apical meristem. We show on the one hand that light is able to activate expression of the stem cell inducer WUSCHEL independently of photosynthesis and that this likely involves inter-regional cytokinin signaling. Metabolic signals, on the other hand, are transduced to the meristem through activation of the TARGET OF RAPAMYCIN (TOR) kinase. Surprisingly, TOR is also required for light signal dependent stem cell activation. Thus, the TOR kinase acts as a central integrator of light and metabolic signals and a key regulator of stem cell activation at the shoot apex.

          DOI: http://dx.doi.org/10.7554/eLife.17023.001

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          Plants are able to grow and develop throughout their lives thanks to groups of stem cells at the tips of their shoots and roots, which can constantly divide to produce new cells. Energy captured from sunlight during a process called photosynthesis is the main source of energy for most plants. Therefore, the amount and quality of light in the environment has a big influence on how plants grow and develop. An enzyme called TOR kinase can sense energy levels in animal cells and regulate many processes including growth and cell division. Plants also have a TOR kinase, but it is less clear if it plays the same role in plants, and whether it can respond to light.

          Plant stem cells only start to divide after the seed germinates. In shoots, a protein called WUSCHEL is required to maintain stem cells in an active state. Here, Pfeiffer et al. studied how shoot stem cells are activated in response to environmental signals in a plant known as Arabidopsis. The experiments show that light is able to activate the production of WUSCHEL independently of photosynthesis via a signal pathway that depends on TOR kinase. The stem cells do not directly sense light; instead other cells detect the light and relay the information to the stem cells with the help of a hormone called cytokinin.

          Further experiments show that information about energy levels in cells is relayed via another signal pathway that also involves the TOR kinase. Therefore, Pfeiffer et al.’s findings suggest that the activation of TOR by light allows plant cells to anticipate how much energy will be available and efficiently tune their growth and development to cope with the environmental conditions. Future challenges are to understand how TOR kinase is regulated by light signals and how this enzyme is able to act on WUSCHEL to trigger stem cell division.

          DOI: http://dx.doi.org/10.7554/eLife.17023.002

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          Most cited references64

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          Local, efflux-dependent auxin gradients as a common module for plant organ formation.

          Plants, compared to animals, exhibit an amazing adaptability and plasticity in their development. This is largely dependent on the ability of plants to form new organs, such as lateral roots, leaves, and flowers during postembryonic development. Organ primordia develop from founder cell populations into organs by coordinated cell division and differentiation. Here, we show that organ formation in Arabidopsis involves dynamic gradients of the signaling molecule auxin with maxima at the primordia tips. These gradients are mediated by cellular efflux requiring asymmetrically localized PIN proteins, which represent a functionally redundant network for auxin distribution in both aerial and underground organs. PIN1 polar localization undergoes a dynamic rearrangement, which correlates with establishment of auxin gradients and primordium development. Our results suggest that PIN-dependent, local auxin gradients represent a common module for formation of all plant organs, regardless of their mature morphology or developmental origin.
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            Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.

            Cytokinins are hormones that regulate cell division and development. As a result of a lack of specific mutants and biochemical tools, it has not been possible to study the consequences of cytokinin deficiency. Cytokinin-deficient plants are expected to yield information about processes in which cytokinins are limiting and that, therefore, they might regulate. We have engineered transgenic Arabidopsis plants that overexpress individually six different members of the cytokinin oxidase/dehydrogenase (AtCKX) gene family and have undertaken a detailed phenotypic analysis. Transgenic plants had increased cytokinin breakdown (30 to 45% of wild-type cytokinin content) and reduced expression of the cytokinin reporter gene ARR5:GUS (beta-glucuronidase). Cytokinin deficiency resulted in diminished activity of the vegetative and floral shoot apical meristems and leaf primordia, indicating an absolute requirement for the hormone. By contrast, cytokinins are negative regulators of root growth and lateral root formation. We show that the increased growth of the primary root is linked to an enhanced meristematic cell number, suggesting that cytokinins control the exit of cells from the root meristem. Different AtCKX-green fluorescent protein fusion proteins were localized to the vacuoles or the endoplasmic reticulum and possibly to the extracellular space, indicating that subcellular compartmentation plays an important role in cytokinin biology. Analyses of promoter:GUS fusion genes showed differential expression of AtCKX genes during plant development, the activity being confined predominantly to zones of active growth. Our results are consistent with the hypothesis that cytokinins have central, but opposite, regulatory functions in root and shoot meristems and indicate that a fine-tuned control of catabolism plays an important role in ensuring the proper regulation of cytokinin functions.
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              PIFs: pivotal components in a cellular signaling hub.

              A small subset of basic helix-loop-helix transcription factors called PIFs (phytochrome-interacting factors) act to repress seed germination, promote seedling skotomorphogenesis and promote shade-avoidance through regulated expression of over a thousand genes. Light-activated phytochrome molecules directly reverse these activities by inducing rapid degradation of the PIF proteins. Here, we review recent advances in dissecting this signaling pathway and examine emerging evidence that indicates that other pathways also converge to regulate PIF activity, including the gibberellin pathway, the circadian clock and high temperature. Thus PIFs have broader roles than previously appreciated, functioning as a cellular signaling hub that integrates multiple signals to orchestrate regulation of the transcriptional network that drives multiple facets of downstream morphogenesis. The relative contributions of the individual PIFs to this spectrum of regulatory functions ranges from quantitatively redundant to qualitatively distinct. Copyright © 2010 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                11 July 2016
                2016
                : 5
                Affiliations
                [1 ]deptDepartment of Stem Cell Biology , Centre for Organismal Studies, Heidelberg University , Heidelberg, Germany
                [2 ]deptDepartment of Molecular Plant Biology , Centre for Organismal Studies, Heidelberg University , Heidelberg, Germany
                [3 ]deptDepartment of Molecular Biology , Max Planck Institute for Developmental Biology , Tübingen, Germany
                [4]University of Lausanne , Switzerland
                [5]University of Lausanne , Switzerland
                Author notes
                [†]

                Graduate School of Life and Enviromental sciences, University of Tsukuba, Tsukuba, Japan.

                [‡]

                Umeå Plant Science Centre, Umeå University, Umeå, Sweden.

                Article
                17023
                10.7554/eLife.17023
                4969040
                27400267
                709b9858-2466-483b-b66b-09f5a7adaf32
                © 2016, Pfeiffer et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100008316, Baden-Württemberg Stiftung;
                Award ID: Eliteprogramme for Postdocs
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: CellNetworks Cluster of Excellence
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: HE 1848/15-1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: WI 3560/1-1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: SFB 1036
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: Starting Grant 282139, StemCellAdapt
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: SFB 873
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Developmental Biology and Stem Cells
                Plant Biology
                Research Article
                Custom metadata
                2.5
                TOR kinase guides the transition of plant stem cells from the dormant embryonic state to the active adult state by integrating light and metabolic signals.

                Life sciences
                tor kinase,light signaling,wuschel,stem cell activation,metabolic signaling,<i>a. thaliana</i>

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