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Organ regeneration does not require a functional stem cell niche in plants.

ABSTRACT: Plants rely on the maintenance of stem cell niches at their apices for the continuous growth of roots and shoots. However, although the developmental plasticity of plant cells has been demonstrated, it is not known whether the stem cell niche is required for organogenesis. Here we explore the capacity of a broad range of differentiating cells to regenerate an organ without the activity of a stem cell niche. Using a root-tip regeneration system in Arabidopsis thaliana to track the molecular and functional recovery of cell fates, we show that re-specification of lost cell identities begins within hours of excision and that the function of specialized cells is restored within one day. Critically, regeneration proceeds in plants with mutations that fail to maintain the stem cell niche. These results show that stem-cell-like properties that mediate complete organ regeneration are dispersed in plant meristems and are not restricted to niches, which nonetheless seem to be necessary for indeterminate growth. This regenerative reprogramming of an entire organ without transition to a stereotypical stem cell environment has intriguing parallels to recent reports of induced transdifferentiation of specific cell types in the adult organs of animals.

SUBMITTER: Sena G

PROVIDER: S-EPMC2649681 | biostudies-literature | 2009 Feb

REPOSITORIES: biostudies-literature

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Organ regeneration does not require a functional stem cell niche in plants.

Sena Giovanni G Wang Xiaoning X Liu Hsiao-Yun HY Hofhuis Hugo H Birnbaum Kenneth D KD

Nature 20090128 7233

Plants rely on the maintenance of stem cell niches at their apices for the continuous growth of roots and shoots. However, although the developmental plasticity of plant cells has been demonstrated, it is not known whether the stem cell niche is required for organogenesis. Here we explore the capacity of a broad range of differentiating cells to regenerate an organ without the activity of a stem cell niche. Using a root-tip regeneration system in Arabidopsis thaliana to track the molecular and f ...[more]

PMID: 19182776

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Project description:A critical step in regeneration is recreating the cellular identities and patterns of lost organs long after embryogenesis is complete. In plants, perpetual (indeterminate) organ growth occurs in apical stem cell niches, which have been shown to re-establish quickly when damaged or removed (1,2). Here we ask whether the machinery of perpetual organ growth, stem cell activity, is needed for the phase of regeneration that leads to replenishing lost cell identities and patterning, or, whether organ re-establishment enlists a wider group of pluripotent cells. We adapt a root tip regeneration system to Arabidopsis that permits us to assess the molecular and functional recovery of specific cell fates during organ regeneration. These results suggest a rapid restoration of missing cell fate and function in advance of the recovery of stem cell activity. Surprisingly, plants with mutations that fail to maintain stem cell activity were able to re-pattern their distal tip and re-specify lost cell fates. Thus, although stem cell activity is required to resume indeterminate growth (3), our results show it is not necessary for cell re-specification and patterning steps. This implies a regeneration mechanism that coordinates patterning of the whole organ, as in embryogenesis, but is initiated from different starting morphologies. 1. Feldman, L. J. Denovo Origin of Quiescent Center Regenerating Root Apices of Zea-Mays. Planta 128, 207-212 (1976). 2. Xu, J. et al. A molecular framework for plant regeneration. Science 311, 385-8 (2006). 3. Gordon, S. P. et al. Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134, 3539-48 (2007). We adapted root tip excision techniques to Arabidopsis, enabling us to perform microarray profiling of regenerating root tissue. Excisions were performed at 4 days post-germination (dpg) at a distance of 130 um from the root tip, resulting in the complete excision of QC, all surrounding stem cells along with several tiers of daughter cells, and the root cap, including all of the columella and most of the lateral root cap. The tip section and then approximately 70 um of regenerating tissue was recut at different time points post cutting. We sampled regenerating stumps at 0hrs, 5 hrs, 13 hrs, 22 hrs, and 7 days after the excision for microarray analysis (Methods). We also sampled root sections immediately above the zone competent to regenerate at 270 um to approximately 340 um. Keywords: time course, development, root regeneration

Project description:A critical step in regeneration is recreating the cellular identities and patterns of lost organs long after embryogenesis is complete. In plants, perpetual (indeterminate) organ growth occurs in apical stem cell niches, which have been shown to re-establish quickly when damaged or removed (1,2). Here we ask whether the machinery of perpetual organ growth, stem cell activity, is needed for the phase of regeneration that leads to replenishing lost cell identities and patterning, or, whether organ re-establishment enlists a wider group of pluripotent cells. We adapt a root tip regeneration system to Arabidopsis that permits us to assess the molecular and functional recovery of specific cell fates during organ regeneration. These results suggest a rapid restoration of missing cell fate and function in advance of the recovery of stem cell activity. Surprisingly, plants with mutations that fail to maintain stem cell activity were able to re-pattern their distal tip and re-specify lost cell fates. Thus, although stem cell activity is required to resume indeterminate growth (3), our results show it is not necessary for cell re-specification and patterning steps. This implies a regeneration mechanism that coordinates patterning of the whole organ, as in embryogenesis, but is initiated from different starting morphologies. 1. Feldman, L. J. Denovo Origin of Quiescent Center Regenerating Root Apices of Zea-Mays. Planta 128, 207-212 (1976). 2. Xu, J. et al. A molecular framework for plant regeneration. Science 311, 385-8 (2006). 3. Gordon, S. P. et al. Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134, 3539-48 (2007). We adapted root tip excision techniques to Arabidopsis, enabling us to perform microarray profiling of regenerating root tissue. Excisions were performed at 4 days post-germination (dpg) at a distance of 130 um from the root tip, resulting in the complete excision of QC, all surrounding stem cells along with several tiers of daughter cells, and the root cap, including all of the columella and most of the lateral root cap. The tip section and then approximately 70 um of regenerating tissue was recut at different time points post cutting. We sampled regenerating stumps at 0hrs, 5 hrs, 13 hrs, 22 hrs, and 7 days after the excision for microarray analysis (Methods). We also sampled root sections immediately above the zone competent to regenerate at 270 um to approximately 340 um. Experiment Overall Design: 30 samples with 4 or 3 replicates for each condition representing a time course of regenerating root stumps and including controls for root tips (regeneration endpoint) at 4 dpg and 8 dpg and a wounded set of samples representing root tissue at 270-340 mm from the root tip for non-regeneration control

Project description:Background: Skeletal muscle crucially depends on motor innervation, and, when damaged, on the resident muscle stem cells (MuSCs). However, the role and function of MuSCs in the context of denervation remains poorly understood. Methods: Alterations of MuSCs and their myofiber niche after denervation were investigated in a surgery-based mouse model of unilateral sciatic nerve transection. FACS-isolated MuSCs were subjected to RNA-sequencing and mass spectrometry for the analysis of intrinsic changes after denervation and in vivo assays, such as Cardiotoxin-induced muscle injury or MuSC transplantation, were performed to assess MuSC functions after denervation. Bioinformatic and histological analyses were conducted to further examine MuSCs and their myofiber niche after denervation. Results: Muscle cross section analysis revealed a significant increase in Pax7 (p-value= 0.0441), Pax7/Ki67 (p-value= 0.0023), MyoD (p-value= 0.0016) and Myog (p-value= 0.0057) positive cells after denervation, illustrating a break of quiescence and commitment to the myogenic lineage. An Omics approach showed profound intrinsic alterations on the mRNA (2613 differentially expressed genes, p-value <0.05) and protein (1096 differentially abundant proteins, q-value <0.05) level of MuSCs 21 days after denervation. Skeletal muscle injury together with denervation surgery caused deregulated regeneration, indicated by the reduced number of proliferating MuSCs and sustained high levels of developmental myosin heavy chain (Sham: 1 % vs DEN: 40 % of all myofibers), at 21 days post-surgery. In a transplantation assay, MuSCs from a denervated host were still able to engraft and fuse to form new myofibers, irrespective of the innervation status of the recipient muscle. Analysis of myofibers revealed not only massive changes in the expression profile (10492 differentially expressed genes, p-value <0.05) after denervation, but it was also shown that secretion of Opn and Tgfb1 from denervated myofibers was increased 30-fold and 6000-fold, respectively. Bioinformatic analyses indicated strong upregulation of gene expression of the transcription factor Junb in MuSCs from denervated muscles (log2 fold change = 3.27). Of interest, Tgfb1 recombinant protein was able to induce Junb gene expression in vitro, demonstrating that myofiber-secreted ligands can induce gene expression changes in MuSCs, which might result in the phenotypes observed after denervation. Conclusion: Skeletal muscle denervation is altering myofiber secretion, causing MuSC activation and profound intrinsic changes, leading to reduced regenerative capacity. As MuSCs possess a remarkable regenerative potential, they might represent a promising target for novel treatment options for neuromuscular disorders and peripheral nerve injuries.

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Organ regeneration does not require a functional stem cell niche in plants.

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Organ regeneration does not require a functional stem cell niche in plants.

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