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      Stem-cell-ubiquitous genes spatiotemporally coordinate division through regulation of stem-cell-specific gene networks

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          Abstract

          Stem cells are responsible for generating all of the differentiated cells, tissues, and organs in a multicellular organism and, thus, play a crucial role in cell renewal, regeneration, and organization. A number of stem cell type-specific genes have a known role in stem cell maintenance, identity, and/or division. Yet, how genes expressed across different stem cell types, referred to here as stem-cell-ubiquitous genes, contribute to stem cell regulation is less understood. Here, we find that, in the Arabidopsis root, a stem-cell-ubiquitous gene, TESMIN-LIKE CXC2 (TCX2), controls stem cell division by regulating stem cell-type specific networks. Development of a mathematical model of TCX2 expression allows us to show that TCX2 orchestrates the coordinated division of different stem cell types. Our results highlight that genes expressed across different stem cell types ensure cross-communication among cells, allowing them to divide and develop harmonically together.

          Abstract

          Stem-cell-specific genes regulate processes such as maintenance, identity and/or division. Here, the authors show that in the Arabidopsis root TCX2, a gene expressed across different stem cell populations (a stem-cell-ubiquitous gene), controls division and identity by regulating stem-cell-type-specific networks.

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          Most cited references30

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          Forcing cells to change lineages.

          The ability to produce stem cells by induced pluripotency (iPS reprogramming) has rekindled an interest in earlier studies showing that transcription factors can directly convert specialized cells from one lineage to another. Lineage reprogramming has become a powerful tool to study cell fate choice during differentiation, akin to inducing mutations for the discovery of gene functions. The lessons learnt provide a rubric for how cells may be manipulated for therapeutic purposes.
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            Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers.

            Throughout the lifespan of a plant, which in some cases can last more than one thousand years, the stem cell niches in the root and shoot apical meristems provide cells for the formation of complete root and shoot systems, respectively. Both niches are superficially different and it has remained unclear whether common regulatory mechanisms exist. Here we address whether root and shoot meristems use related factors for stem cell maintenance. In the root niche the quiescent centre cells, surrounded by the stem cells, express the homeobox gene WOX5 (WUSCHEL-RELATED HOMEOBOX 5), a homologue of the WUSCHEL (WUS) gene that non-cell-autonomously maintains stem cells in the shoot meristem. Loss of WOX5 function in the root meristem stem cell niche causes terminal differentiation in distal stem cells and, redundantly with other regulators, also provokes differentiation of the proximal meristem. Conversely, gain of WOX5 function blocks differentiation of distal stem cell descendents that normally differentiate. Importantly, both WOX5 and WUS maintain stem cells in either a root or shoot context. Together, our data indicate that stem cell maintenance signalling in both meristems employs related regulators.
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              The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling.

              Asymmetric cell divisions play an important role in the establishment and propagation of the cellular pattern of plant tissues. The SHORT-ROOT (SHR) gene is required for the asymmetric cell division responsible for formation of ground tissue (endodermis and cortex) as well as specification of endodermis in the Arabidopsis root. We show that SHR encodes a putative transcription factor with homology to SCARECROW (SCR). From analyses of gene expression and cell identity in genetically stable and unstable alleles of shr, we conclude that SHR functions upstream of SCR and participates in a radial signaling pathway. Consistent with a regulatory role in radial patterning, ectopic expression of SHR results in supernumerary cell divisions and abnormal cell specification in the root meristem.
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                Author and article information

                Contributors
                ross_sozzani@ncsu.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                6 December 2019
                6 December 2019
                2019
                : 10
                : 5574
                Affiliations
                [1 ]ISNI 0000 0001 2173 6074, GRID grid.40803.3f, Department of Plant and Microbial Biology, , North Carolina State University, ; Raleigh, NC 27695 United States
                [2 ]ISNI 0000 0001 2173 6074, GRID grid.40803.3f, Biomathematics Graduate Program, , North Carolina State University, ; Raleigh, NC 27695 United States
                [3 ]ISNI 0000 0001 2173 6074, GRID grid.40803.3f, Department of Electrical and Computer Engineering, , North Carolina State University, ; Raleigh, NC 27695 United States
                [4 ]ISNI 0000000419368956, GRID grid.168010.e, Department of Biology, , Stanford University, ; Stanford, CA 94305 United States
                [5 ]ISNI 0000 0001 2185 2366, GRID grid.255014.7, Department of Biology, , Denison University, ; Granville, OH 43023 United States
                [6 ]ISNI 0000000419368956, GRID grid.168010.e, Howard Hughes Medical Institute (HHMI), , Stanford University, ; Stanford, CA 94305 United States
                [7 ]ISNI 0000 0004 1936 7312, GRID grid.34421.30, Present Address: Department of Plant Pathology and Microbiology, , Iowa State University, ; Ames, IA 50011 United States
                Author information
                http://orcid.org/0000-0002-8099-0483
                Article
                13132
                10.1038/s41467-019-13132-2
                6897965
                31811116
                1c656a6d-5e02-4c34-99f8-f22706bdc619
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 21 December 2018
                : 19 October 2019
                Funding
                Funded by: GAAN Fellowship in Molecular Biotechnology (grant #P200A160061).
                Funded by: FundRef https://doi.org/10.13039/100000001, National Science Foundation (NSF);
                Award ID: DGE-1252376
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000002, U.S. Department of Health & Human Services | National Institutes of Health (NIH);
                Award ID: NIH5T32GM007276
                Award Recipient :
                Funded by: Donald Kennedy Fellowship
                Funded by: Integrated Molecular Plant Systems Research Experience for Undergraduates (IMPS REU)
                Funded by: FundRef https://doi.org/10.13039/100000011, Howard Hughes Medical Institute (HHMI);
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                gene regulatory networks,plant stem cell,self-renewal
                Uncategorized
                gene regulatory networks, plant stem cell, self-renewal

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