A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetic stem cell division

A. Cruz-Ramirez; S. Diaz-Trivino; I. Blilou; R. Benjamins; Y. Long; B.J.G. Scheres

doi:10.1016/j.cell.2012.07.017

A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetic stem cell division

A. Cruz-Ramirez, S. Diaz-Trivino, I. Blilou, R. Benjamins, Y. Long, B.J.G. Scheres

Plant Developmental Biology

Research output: Contribution to journal › Article › Academic › peer-review

180 Citations (Scopus)

Abstract

In plants, where cells cannot migrate, asymmetric cell divisions (ACDs) must be confined to the appropriate spatial context. We investigate tissue-generating asymmetric divisions in a stem cell daughter within the Arabidopsis root. Spatial restriction of these divisions requires physical binding of the stem cell regulator SCARECROW (SCR) by the RETINOBLASTOMA-RELATED (RBR) protein. In the stem cell niche, SCR activity is counteracted by phosphorylation of RBR through a cyclinD6;1-CDK complex. This cyclin is itself under transcriptional control of SCR and its partner SHORT ROOT (SHR), creating a robust bistable circuit with either high or low SHR-SCR complex activity. Auxin biases this circuit by promoting CYCD6;1 transcription. Mathematical modeling shows that ACDs are only switched on after integration of radial and longitudinal information, determined by SHR and auxin distribution, respectively. Coupling of cell-cycle progression to protein degradation resets the circuit, resulting in a “flip flop” that constrains asymmetric cell division to the stem cell region.

Original language	English
Pages (from-to)	1002-1015
Journal	Cell
Volume	150
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2012.07.017
Publication status	Published - 2012

Keywords

protein-protein interactions
arabidopsis root-meristem
tumor-suppressor
split luciferase
auxin transport
cycle
gene
differentiation
plants
growth

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title = "A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetic stem cell division",

abstract = "In plants, where cells cannot migrate, asymmetric cell divisions (ACDs) must be confined to the appropriate spatial context. We investigate tissue-generating asymmetric divisions in a stem cell daughter within the Arabidopsis root. Spatial restriction of these divisions requires physical binding of the stem cell regulator SCARECROW (SCR) by the RETINOBLASTOMA-RELATED (RBR) protein. In the stem cell niche, SCR activity is counteracted by phosphorylation of RBR through a cyclinD6;1-CDK complex. This cyclin is itself under transcriptional control of SCR and its partner SHORT ROOT (SHR), creating a robust bistable circuit with either high or low SHR-SCR complex activity. Auxin biases this circuit by promoting CYCD6;1 transcription. Mathematical modeling shows that ACDs are only switched on after integration of radial and longitudinal information, determined by SHR and auxin distribution, respectively. Coupling of cell-cycle progression to protein degradation resets the circuit, resulting in a “flip flop” that constrains asymmetric cell division to the stem cell region.",

keywords = "protein-protein interactions, arabidopsis root-meristem, tumor-suppressor, split luciferase, auxin transport, cycle, gene, differentiation, plants, growth",

author = "A. Cruz-Ramirez and S. Diaz-Trivino and I. Blilou and R. Benjamins and Y. Long and B.J.G. Scheres",

year = "2012",

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T1 - A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetic stem cell division

AU - Cruz-Ramirez, A.

AU - Diaz-Trivino, S.

AU - Blilou, I.

AU - Benjamins, R.

AU - Long, Y.

AU - Scheres, B.J.G.

PY - 2012

Y1 - 2012

N2 - In plants, where cells cannot migrate, asymmetric cell divisions (ACDs) must be confined to the appropriate spatial context. We investigate tissue-generating asymmetric divisions in a stem cell daughter within the Arabidopsis root. Spatial restriction of these divisions requires physical binding of the stem cell regulator SCARECROW (SCR) by the RETINOBLASTOMA-RELATED (RBR) protein. In the stem cell niche, SCR activity is counteracted by phosphorylation of RBR through a cyclinD6;1-CDK complex. This cyclin is itself under transcriptional control of SCR and its partner SHORT ROOT (SHR), creating a robust bistable circuit with either high or low SHR-SCR complex activity. Auxin biases this circuit by promoting CYCD6;1 transcription. Mathematical modeling shows that ACDs are only switched on after integration of radial and longitudinal information, determined by SHR and auxin distribution, respectively. Coupling of cell-cycle progression to protein degradation resets the circuit, resulting in a “flip flop” that constrains asymmetric cell division to the stem cell region.

AB - In plants, where cells cannot migrate, asymmetric cell divisions (ACDs) must be confined to the appropriate spatial context. We investigate tissue-generating asymmetric divisions in a stem cell daughter within the Arabidopsis root. Spatial restriction of these divisions requires physical binding of the stem cell regulator SCARECROW (SCR) by the RETINOBLASTOMA-RELATED (RBR) protein. In the stem cell niche, SCR activity is counteracted by phosphorylation of RBR through a cyclinD6;1-CDK complex. This cyclin is itself under transcriptional control of SCR and its partner SHORT ROOT (SHR), creating a robust bistable circuit with either high or low SHR-SCR complex activity. Auxin biases this circuit by promoting CYCD6;1 transcription. Mathematical modeling shows that ACDs are only switched on after integration of radial and longitudinal information, determined by SHR and auxin distribution, respectively. Coupling of cell-cycle progression to protein degradation resets the circuit, resulting in a “flip flop” that constrains asymmetric cell division to the stem cell region.

KW - protein-protein interactions

KW - arabidopsis root-meristem

KW - tumor-suppressor

KW - split luciferase

KW - auxin transport

KW - cycle

KW - gene

KW - differentiation

KW - plants

KW - growth

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DO - 10.1016/j.cell.2012.07.017

M3 - Article

VL - 150

SP - 1002

EP - 1015

JO - Cell

JF - Cell

SN - 0092-8674

IS - 5

ER -