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

Alfredo Cruz-Ramírez; Sara Díaz-Triviño; Ikram Blilou; Verônica A Grieneisen; Rosangela Sozzani; Christos Zamioudis; Pál Miskolczi; Jeroen Nieuwland; René Benjamins; Pankaj Dhonukshe; Juan Caballero-Pérez; Beatrix Horvath; Yuchen Long; Ari Pekka Mähönen; Hongtao Zhang; Jian Xu; James A H Murray; Philip N Benfey; Laszlo Bako; Athanasius F M Marée; Ben Scheres

doi:10.1016/j.cell.2012.07.017

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

Alfredo Cruz-Ramírez, Sara Díaz-Triviño, Ikram Blilou, Verônica A Grieneisen, Rosangela Sozzani, Christos Zamioudis, Pál Miskolczi, Jeroen Nieuwland, René Benjamins, Pankaj Dhonukshe, Juan Caballero-Pérez, Beatrix Horvath, Yuchen Long, Ari Pekka Mähönen, Hongtao Zhang, Jian Xu, James A H Murray, Philip N Benfey, Laszlo Bako, Athanasius F M MaréeBen Scheres

Faculty of Computing, Engineering and Science

Research output: Contribution to journal › Article › 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)	1002-15
Number of pages	14
Journal	Cell
Volume	150
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2012.07.017
Publication status	Published - 31 Aug 2012

Keywords

Amino Acid Sequence
Arabidopsis
Arabidopsis Proteins
Asymmetric Cell Division
Cyclin D
Cyclin-Dependent Kinases
Indoleacetic Acids
Mesophyll Cells
Molecular Sequence Data
Phosphorylation
Plant Roots
Sequence Alignment

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Cruz-Ramírez, A., Díaz-Triviño, S., Blilou, I., Grieneisen, V. A., Sozzani, R., Zamioudis, C., Miskolczi, P., Nieuwland, J., Benjamins, R., Dhonukshe, P., Caballero-Pérez, J., Horvath, B., Long, Y., Mähönen, A. P., Zhang, H., Xu, J., Murray, J. A. H., Benfey, P. N., Bako, L., ... Scheres, B. (2012). A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell, 150(5), 1002-15. https://doi.org/10.1016/j.cell.2012.07.017

@article{d04867a697c54112b7cb25679d1f6f68,

title = "A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues 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.",

keywords = "Amino Acid Sequence, Arabidopsis, Arabidopsis Proteins, Asymmetric Cell Division, Cyclin D, Cyclin-Dependent Kinases, Indoleacetic Acids, Mesophyll Cells, Molecular Sequence Data, Phosphorylation, Plant Roots, Sequence Alignment",

author = "Alfredo Cruz-Ram{\'i}rez and Sara D{\'i}az-Trivi{\~n}o and Ikram Blilou and Grieneisen, {Ver{\^o}nica A} and Rosangela Sozzani and Christos Zamioudis and P{\'a}l Miskolczi and Jeroen Nieuwland and Ren{\'e} Benjamins and Pankaj Dhonukshe and Juan Caballero-P{\'e}rez and Beatrix Horvath and Yuchen Long and M{\"a}h{\"o}nen, {Ari Pekka} and Hongtao Zhang and Jian Xu and Murray, {James A H} and Benfey, {Philip N} and Laszlo Bako and Mar{\'e}e, {Athanasius F M} and Ben Scheres",

year = "2012",

month = aug,

day = "31",

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

language = "English",

volume = "150",

pages = "1002--15",

journal = "Cell",

issn = "0092-8674",

publisher = "Elsevier",

number = "5",

}

Cruz-Ramírez, A, Díaz-Triviño, S, Blilou, I, Grieneisen, VA, Sozzani, R, Zamioudis, C, Miskolczi, P, Nieuwland, J, Benjamins, R, Dhonukshe, P, Caballero-Pérez, J, Horvath, B, Long, Y, Mähönen, AP, Zhang, H, Xu, J, Murray, JAH, Benfey, PN, Bako, L, Marée, AFM & Scheres, B 2012, 'A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division', Cell, vol. 150, no. 5, pp. 1002-15. https://doi.org/10.1016/j.cell.2012.07.017

TY - JOUR

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

AU - Cruz-Ramírez, Alfredo

AU - Díaz-Triviño, Sara

AU - Blilou, Ikram

AU - Grieneisen, Verônica A

AU - Sozzani, Rosangela

AU - Zamioudis, Christos

AU - Miskolczi, Pál

AU - Nieuwland, Jeroen

AU - Benjamins, René

AU - Dhonukshe, Pankaj

AU - Caballero-Pérez, Juan

AU - Horvath, Beatrix

AU - Long, Yuchen

AU - Mähönen, Ari Pekka

AU - Zhang, Hongtao

AU - Xu, Jian

AU - Murray, James A H

AU - Benfey, Philip N

AU - Bako, Laszlo

AU - Marée, Athanasius F M

AU - Scheres, Ben

PY - 2012/8/31

Y1 - 2012/8/31

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 - Amino Acid Sequence

KW - Arabidopsis

KW - Arabidopsis Proteins

KW - Asymmetric Cell Division

KW - Cyclin D

KW - Cyclin-Dependent Kinases

KW - Indoleacetic Acids

KW - Mesophyll Cells

KW - Molecular Sequence Data

KW - Phosphorylation

KW - Plant Roots

KW - Sequence Alignment

U2 - 10.1016/j.cell.2012.07.017

DO - 10.1016/j.cell.2012.07.017

M3 - Article

C2 - 22921914

SN - 0092-8674

VL - 150

SP - 1002

EP - 1015

JO - Cell

JF - Cell

IS - 5

ER -

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

Abstract

Keywords

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