A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cue to inform asymmetric stem cell division

L.A. Cruz Ramirez; S. Diaz-Trivino; I. Blilou; V Grieneisen; R. Sozzani; C Zamioudis; P. Miskolczi; J. Nieuwland; R. Benjamins; P.B. Dhonukshe; J. Caballero-Pérez; B.M. Horvath; Y. Long; A.P. Mähönen; H. Zhang; J. Xu; J.A.H. Murray; P.N. Benfey; L. Bako; A.F.M. Marée; B.J.G. Scheres

doi:10.1016/j.cell.2012.07.017

A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cue to inform asymmetric stem cell division

L.A. Cruz Ramirez
, S. Diaz-Trivino
, I. Blilou
, V Grieneisen
, R. Sozzani
, C Zamioudis
, P. Miskolczi
, J. Nieuwland
, R. Benjamins
, P.B. Dhonukshe
, J. Caballero-Pérez
, B.M. Horvath
, Y. Long
, A.P. Mähönen
, H. Zhang
, J. Xu
, J.A.H. Murray
, P.N. Benfey
, L. Bako
, A.F.M. Marée

B.J.G. Scheres

extern

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

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
Number of pages	14
Journal	Cell
Volume	150
DOIs	https://doi.org/10.1016/j.cell.2012.07.017
Publication status	Published - 2012

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Cruz Ramirez, L. A., Diaz-Trivino, S., Blilou, I., Grieneisen, V., Sozzani, R., Zamioudis, C., Miskolczi, P., Nieuwland, J., Benjamins, R., Dhonukshe, P. B., Caballero-Pérez, J., Horvath, B. M., Long, Y., Mähönen, A. P., Zhang, H., Xu, J., Murray, J. A. H., Benfey, P. N., Bako, L., ... Scheres, B. J. G. (2012). A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cue to inform asymmetric stem cell division. Cell, 150, 1002-1015. https://doi.org/10.1016/j.cell.2012.07.017

@article{842f45463538435f9e5c03d456acb457,

title = "A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cue to inform asymmetric 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.",

author = "\{Cruz Ramirez\}, L.A. and S. Diaz-Trivino and I. Blilou and V Grieneisen and R. Sozzani and C Zamioudis and P. Miskolczi and J. Nieuwland and R. Benjamins and P.B. Dhonukshe and J. Caballero-P{\'e}rez and B.M. Horvath and Y. Long and A.P. M{\"a}h{\"o}nen and H. Zhang and J. Xu and J.A.H. Murray and P.N. Benfey and L. Bako and A.F.M. Mar{\'e}e and B.J.G. Scheres",

year = "2012",

doi = "10.1016/j.cell.2012.07.017",

language = "English",

volume = "150",

pages = "1002--1015",

journal = "Cell",

issn = "0092-8674",

publisher = "Elsevier BV",

}

Cruz Ramirez, LA, Diaz-Trivino, S, Blilou, I, Grieneisen, V, Sozzani, R, Zamioudis, C, Miskolczi, P, Nieuwland, J, Benjamins, R, Dhonukshe, PB, Caballero-Pérez, J, Horvath, BM, Long, Y, Mähönen, AP, Zhang, H, Xu, J, Murray, JAH, Benfey, PN, Bako, L, Marée, AFM & Scheres, BJG 2012, 'A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cue to inform asymmetric stem cell division', Cell, vol. 150, pp. 1002-1015. https://doi.org/10.1016/j.cell.2012.07.017

TY - JOUR

T1 - A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cue to inform asymmetric stem cell division

AU - Cruz Ramirez, L.A.

AU - Diaz-Trivino, S.

AU - Blilou, I.

AU - Grieneisen, V

AU - Sozzani, R.

AU - Zamioudis, C

AU - Miskolczi, P.

AU - Nieuwland, J.

AU - Benjamins, R.

AU - Dhonukshe, P.B.

AU - Caballero-Pérez, J.

AU - Horvath, B.M.

AU - Long, Y.

AU - Mähönen, A.P.

AU - Zhang, H.

AU - Xu, J.

AU - Murray, J.A.H.

AU - Benfey, P.N.

AU - Bako, L.

AU - Marée, A.F.M.

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.

U2 - 10.1016/j.cell.2012.07.017

DO - 10.1016/j.cell.2012.07.017

M3 - Article

SN - 0092-8674

VL - 150

SP - 1002

EP - 1015

JO - Cell

JF - Cell

ER -

A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cue to inform asymmetric stem cell division

Abstract

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