A SCARECROW-RETINOBLASTOMA Protein Network Controls Protective Quiescence in the Arabidopsis Root Stem Cell Organizer

Cruz‐Ramírez, Alfredo; Díaz-Triviño, Sara; Wachsman, Guy; Du, Yujuan; Arteaga-Vázquez, Mario; Zhang, Hongtao; Benjamins, René; Blilou, Ikram; Neef, Anne B.; Chandler, Vicki L.; Scheres, Ben

doi:10.1371/journal.pbio.1001724

Cited by 146 publications

(200 citation statements)

References 51 publications

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“…Additionally, RAM identity and patterning are tightly linked to cell division regulation. For instance, RETINOBLASTOMA-RELATED interacts with SCR to regulate quiescence in the QC by repressing an asymmetric cell division that generates short-term stem cells (Cruz-Ramírez et al, 2013). The cell cycle switch gene CCS52A (an activator of the anaphase promoting complex/cyclosome [APC/C]) regulates the identity of the QC by repressing mitotic activity in these cells (Vanstraelen et al, 2009).…”

Section: Discussion Rangap Mutant Developmental Phenotypes Are Indepementioning

confidence: 99%

GAP Activity, but Not Subcellular Targeting, Is Required for Arabidopsis RanGAP Cellular and Developmental Functions

et al. 2015

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The Ran GTPase activating protein (RanGAP) is important to Ran signaling involved in nucleocytoplasmic transport, spindle organization, and postmitotic nuclear assembly. Unlike vertebrate and yeast RanGAP, plant RanGAP has an N-terminal WPP domain, required for nuclear envelope association and several mitotic locations of Arabidopsis thaliana RanGAP1. A double null mutant of the two Arabidopsis RanGAP homologs is gametophyte lethal. Here, we created a series of mutants with various reductions in RanGAP levels by combining a RanGAP1 null allele with different RanGAP2 alleles. As RanGAP level decreases, the severity of developmental phenotypes increases, but nuclear import is unaffected. To dissect whether the GAP activity and/or the subcellular localization of RanGAP are responsible for the observed phenotypes, this series of rangap mutants were transformed with RanGAP1 variants carrying point mutations abolishing the GAP activity and/or the WPPdependent subcellular localization. The data show that plant development is differentially affected by RanGAP mutant allele combinations of increasing severity and requires the GAP activity of RanGAP, while the subcellular positioning of RanGAP is dispensable. In addition, our results indicate that nucleocytoplasmic trafficking can tolerate both partial depletion of RanGAP and delocalization of RanGAP from the nuclear envelope.

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Section: Discussion Rangap Mutant Developmental Phenotypes Are Indepementioning

confidence: 99%

GAP Activity, but Not Subcellular Targeting, Is Required for Arabidopsis RanGAP Cellular and Developmental Functions

et al. 2015

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“…A decrease in GRF levels blurred this sharp transition: periclinal cell divisions, which are typical of stem cells, were observed among TACs, whereas markers of the QC and the stem cells extended their expression into the meristem. Cells in the SCN also proliferate at a much slower frequency than the surrounding transit-amplifying meristematic cells (Dolan et al, 1993;Kerk et al, 2000;Campilho et al, 2006;Cruz-Ramírez et al, 2013;Heyman et al, 2013), and a modification of the GRF levels in TACs modified the cell cycle length accordingly.…”

Section: Grfs Repress Stem Cell-like Properties In Tacsmentioning

confidence: 99%

MicroRNA miR396 Regulates the Switch between Stem Cells and Transit-Amplifying Cells in Arabidopsis Roots

et al. 2015

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To ensure an adequate organ mass, the daughters of stem cells progress through a transit-amplifying phase displaying rapid cell division cycles before differentiating. Here, we show that Arabidopsis thaliana microRNA miR396 regulates the transition of root stem cells into transit-amplifying cells by interacting with GROWTH-REGULATING FACTORs (GRFs). The GRFs are expressed in transit-amplifying cells but are excluded from the stem cells through inhibition by miR396. Inactivation of the GRFs increases the meristem size and induces periclinal formative divisions in transit-amplifying cells. The GRFs repress PLETHORA (PLT) genes, regulating their spatial expression gradient. Conversely, PLT activates MIR396 in the stem cells to repress the GRFs. We identified a pathway regulated by GRF transcription factors that represses stem cell-promoting genes in actively proliferating cells, which is essential for the progression of the cell cycle and the orientation of the cell division plane. If unchecked, the expression of the GRFs in the stem cell niche suppresses formative cell divisions and distorts the organization of the quiescent center. We propose that the interactions identified here between miR396 and GRF and PLT transcription factors are necessary to establish the boundary between the stem cell niche and the transit-amplifying region.

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“…To investigate a possible role of RBR in the regulation of cell differentiation in the TZ, we used transgenic lines with reduced levels of RBR due to the expression of an artificial microRNA for gene-silencing overcome (amiGO) targeting the RBR sequence under the 35S promoter (35S pro :amiGORBR) (Cruz-Ramírez et al, 2013). 35S pro :amiGORBR roots displayed an enlarged meristem with an increased number of meristematic cells that resulted in longer roots ( Figures 1B, 1E, and 1F; see Supplemental Figure 1B online), suggesting that RBR acts as a negative regulator of root meristem size and root growth.…”

Section: Rbr Influences Root Meristem Sizementioning

confidence: 99%

RETINOBLASTOMA-RELATED Protein Stimulates Cell Differentiation in theArabidopsisRoot Meristem by Interacting with Cytokinin Signaling

Perilli¹,

Pérez-Pérez

Mambro³

et al. 2013

The Plant Cell

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Maintenance of mitotic cell clusters such as meristematic cells depends on their capacity to maintain the balance between cell division and cell differentiation necessary to control organ growth. In the Arabidopsis thaliana root meristem, the antagonistic interaction of two hormones, auxin and cytokinin, regulates this balance by positioning the transition zone, where mitotically active cells lose their capacity to divide and initiate their differentiation programs. In animals, a major regulator of both cell division and cell differentiation is the tumor suppressor protein RETINOBLASTOMA. Here, we show that similarly to its homolog in animal systems, the plant RETINOBLASTOMA-RELATED (RBR) protein regulates the differentiation of meristematic cells at the transition zone by allowing mRNA accumulation of AUXIN RESPONSE FACTOR19 (ARF19), a transcription factor involved in cell differentiation. We show that both RBR and the cytokinin-dependent transcription factor ARABIDOPSIS RESPONSE REGULATOR12 are required to activate the transcription of ARF19, which is involved in promoting cell differentiation and thus root growth.

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A SCARECROW-RETINOBLASTOMA Protein Network Controls Protective Quiescence in the Arabidopsis Root Stem Cell Organizer

Abstract: Ben Scheres and colleagues report that in the growing tip of plant roots, a gene regulatory network that includes the plant homologue of Retinoblastoma regulates the divisions of long-term stem cells to replenish tissue and to protect the root stem cell niche.

Cited by 146 publications

References 51 publications

GAP Activity, but Not Subcellular Targeting, Is Required for Arabidopsis RanGAP Cellular and Developmental Functions

GAP Activity, but Not Subcellular Targeting, Is Required for Arabidopsis RanGAP Cellular and Developmental Functions

MicroRNA miR396 Regulates the Switch between Stem Cells and Transit-Amplifying Cells in Arabidopsis Roots

RETINOBLASTOMA-RELATED Protein Stimulates Cell Differentiation in theArabidopsisRoot Meristem by Interacting with Cytokinin Signaling

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