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      Control of plant cell fate transitions by transcriptional and hormonal signals

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          Abstract

          Plant meristems carry pools of continuously active stem cells, whose activity is controlled by developmental and environmental signals. After stem cell division, daughter cells that exit the stem cell domain acquire transit amplifying cell identity before they are incorporated into organs and differentiate. In this study, we used an integrated approach to elucidate the role of HECATE ( HEC) genes in regulating developmental trajectories of shoot stem cells in Arabidopsis thaliana. Our work reveals that HEC function stabilizes cell fate in distinct zones of the shoot meristem thereby controlling the spatio-temporal dynamics of stem cell differentiation. Importantly, this activity is concomitant with the local modulation of cellular responses to cytokinin and auxin, two key phytohormones regulating cell behaviour. Mechanistically, we show that HEC factors transcriptionally control and physically interact with MONOPTEROS (MP), a key regulator of auxin signalling, and modulate the autocatalytic stabilization of auxin signalling output.

          eLife digest

          Unlike animals, plants continuously generate new organs that make up their body. At the core of this amazing capacity lie tissues called meristems, which are found at the growing tips of all plants. Meristems contain dividing stem cells. The daughters of these stem cells pass through nearby regions called transition domains. Over time, they change – or differentiate – to go on to become part of tissues like leaves, roots, stems, shoots, flowers or fruits.

          Stem cell differentiation has a direct impact on a plant’s architecture and eventually its reproductive success. For crops, these factors determine yield. This means that understanding this aspect of plant development is central to basic and applied plant biology. Many factors required for shoot meristem activity have been identified, with a focus so far on the processes that control the identity of the cells produced.

          Now, Gaillochet et al. have asked which genes are responsible for controlling when stem cells in meristems differentiate. The analysis focused on the meristem that makes all the above ground parts of model plant Arabidopsis thaliana – the shoot apical meristem. Gaillochet et al. found that HECATE genes (or HEC for short) control the timing of stem cell differentiation by regulating the balance between the activities of two plant hormones: cytokinin and auxin. These genes promote cytokinin signals at the centre of the meristem, and dampen auxin response at the edges. This acts to slow down cell differentiation in two key transition domains of the shoot meristem.

          These new findings provide a molecular framework that now can be further investigated in crop plants to try to improve their yield. The findings also lay the foundation for studies of animals that may define common principles shared among stem cell systems in organisms that diverged over a billion years ago.

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          Most cited references62

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

          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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            An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus.

            Transient gene expression is a fast, flexible and reproducible approach to high-level expression of useful proteins. In plants, recombinant strains of Agrobacterium tumefaciens can be used for transient expression of genes that have been inserted into the T-DNA region of the bacterial Ti plasmid. A bacterial culture is vacuum-infiltrated into leaves, and upon T-DNA transfer, there is ectopic expression of the gene of interest in the plant cells. However, the utility of the system is limited because the ectopic protein expression ceases after 2-3 days. Here, we show that post-transcriptional gene silencing (PTGS) is a major cause for this lack of efficiency. We describe a system based on co-expression of a viral-encoded suppressor of gene silencing, the p19 protein of tomato bushy stunt virus (TBSV), that prevents the onset of PTGS in the infiltrated tissues and allows high level of transient expression. Expression of a range of proteins was enhanced 50-folds or more in the presence of p19 so that protein purification could be achieved from as little as 100 mg of infiltrated leaf material. The effect of p19 was not saturated in cells that had received up to four individual T-DNAs and persisted until leaf senescence. Because of its simplicity and rapidity, we anticipate that the p19-enhanced expression system will have value in industrial production as well as a research tool for isolation and biochemical characterisation of a broad range of proteins without the need for the time-consuming regeneration of stably transformed plants.
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              Fundamental properties of unperturbed haematopoiesis from stem cells in vivo.

              Haematopoietic stem cells (HSCs) are widely studied by HSC transplantation into immune- and blood-cell-depleted recipients. Single HSCs can rebuild the system after transplantation. Chromosomal marking, viral integration and barcoding of transplanted HSCs suggest that very low numbers of HSCs perpetuate a continuous stream of differentiating cells. However, the numbers of productive HSCs during normal haematopoiesis, and the flux of differentiating progeny remain unknown. Here we devise a mouse model allowing inducible genetic labelling of the most primitive Tie2(+) HSCs in bone marrow, and quantify label progression along haematopoietic development by limiting dilution analysis and data-driven modelling. During maintenance of the haematopoietic system, at least 30% or ∼5,000 HSCs are productive in the adult mouse after label induction. However, the time to approach equilibrium between labelled HSCs and their progeny is surprisingly long, a time scale that would exceed the mouse's life. Indeed, we find that adult haematopoiesis is largely sustained by previously designated 'short-term' stem cells downstream of HSCs that nearly fully self-renew, and receive rare but polyclonal HSC input. By contrast, in fetal and early postnatal life, HSCs are rapidly used to establish the immune and blood system. In the adult mouse, 5-fluoruracil-induced leukopenia enhances the output of HSCs and of downstream compartments, thus accelerating haematopoietic flux. Label tracing also identifies a strong lineage bias in adult mice, with several-hundred-fold larger myeloid than lymphoid output, which is only marginally accentuated with age. Finally, we show that transplantation imposes severe constraints on HSC engraftment, consistent with the previously observed oligoclonal HSC activity under these conditions. Thus, we uncover fundamental differences between the normal maintenance of the haematopoietic system, its regulation by challenge, and its re-establishment after transplantation. HSC fate mapping and its linked modelling provide a quantitative framework for studying in situ the regulation of haematopoiesis in health and disease.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                23 October 2017
                2017
                : 6
                : e30135
                Affiliations
                [1 ]deptDepartment of Stem Cell Biology, Centre for Organismal Studies University of Heidelberg HeidelbergGermany
                [2 ]deptInstitute of Applied Mathematics Heidelberg University HeidelbergGermany
                [3 ]deptInterdisciplinary Center for Scientific Computing Heidelberg University HeidelbergGermany
                [4 ]deptDivision of Biological Sciences, Section of Cell and Developmental Biology University of California, San Diego San DiegoUnited States
                [5 ]deptBioquant Center Heidelberg University HeidelbergGermany
                Stanford University/HHMI United States
                Stanford University/HHMI United States
                Author notes
                [‡]

                Max-Planck-Institut für Molekulare Pflanzenphysiologie, Potsdam, Germany.

                [†]

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0003-0537-1356
                http://orcid.org/0000-0001-9686-9197
                http://orcid.org/0000-0002-8229-1555
                http://orcid.org/0000-0001-6825-6297
                https://orcid.org/0000-0003-2581-672X
                https://orcid.org/0000-0002-6406-7066
                http://orcid.org/0000-0002-5831-6505
                http://orcid.org/0000-0003-3667-187X
                Article
                30135
                10.7554/eLife.30135
                5693117
                29058667
                a4661cad-5c38-449b-823f-4574a5583fa8
                © 2017, Gaillochet 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.

                History
                : 03 July 2017
                : 22 October 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: SFB873
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004895, European Social Fund;
                Award ID: Elite program for postdocs
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100008316, Baden-Württemberg Stiftung;
                Award ID: Elite program for postdocs
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 1R01GM112976-01A1
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Developmental Biology and Stem Cells
                Plant Biology
                Custom metadata
                HEC transcription factors control the timing of cell fate transitions in a dynamic stem cell system, allowing plants to adapt their developmental program to diverse environments.

                Life sciences
                hecate1,auxin,cytokinin,shoot meristem,cell fate,a. thaliana
                Life sciences
                hecate1, auxin, cytokinin, shoot meristem, cell fate, a. thaliana

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