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.

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Most cited references 65

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

Eva Benková, Marta Michniewicz, Michael Sauer … (2003)

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.

Tomáš Werner, Václav Motyka, Valérie Laucou … (2003)

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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The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes.

H Schoof, M Lenhard, A Haecker … (2000)

The higher-plant shoot meristem is a dynamic structure whose maintenance depends on the coordination of two antagonistic processes, organ initiation and self-renewal of the stem cell population. In Arabidopsis shoot and floral meristems, the WUSCHEL (WUS) gene is required for stem cell identity, whereas the CLAVATA1, 2, and 3 (CLV) genes promote organ initiation. Our analysis of the interactions between these key regulators indicates that (1) the CLV genes repress WUS at the transcript level and that (2) WUS expression is sufficient to induce meristem cell identity and the expression of the stem cell marker CLV3. Our data suggest that the shoot meristem has properties of a self-regulatory system in which WUS/CLV interactions establish a feedback loop between the stem cells and the underlying organizing center.

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Author and article information

Journal

Journal ID (iso-abbrev): Elife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

ISSN (Print): 2050-084X

Publication date (Electronic): July 11 2016

Volume: 5

Affiliations

[1 ] Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany.

[2 ] Department of Molecular Plant Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany.

[3 ] Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.

Article

DOI: 10.7554/eLife.17023

PMC ID: 4969040

PubMed ID: 27400267

SO-VID: 709b9858-2466-483b-b66b-09f5a7adaf32

History

Keywords: a. thaliana,TOR kinase,WUSCHEL,developmental biology,light signaling,metabolic signaling,plant biology,stem cell activation,stem cells

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Keywords: a. thaliana, TOR kinase, WUSCHEL, developmental biology, light signaling, metabolic signaling, plant biology, stem cell activation, stem cells

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

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Most cited references 65

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

Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.

The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes.

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