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. Marée^*Ben Scheres

^*Corresponding author for this work

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

249 Scopus citations

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 (US)
Pages (from-to)	1002-1015
Number of pages	14
Journal	Cell
Volume	150
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2012.07.017
State	Published - Aug 31 2012
Externally published	Yes

Bibliographical note

Funding Information:
We thank Dominique Bergmann for critically reviewing this manuscript; Fred Sack, Lieven de Veylder, Naohiro Kato, Dorus Gadella, Joachim Goedhart, Tom Beeckman, and Tom Bennett for materials; and Anahí Pérez-Torres, Luis Herrera-Estrella, and Juan Carlos del Pozo for technical advice. B.S. was supported by an ERC Advanced Investigator Fellowship and by ALW-ERAPG grant 855.50.017. A.C.-R. was supported by EMBO-ALTF 1114-2006 and CONACYT 000000000092916 grants. S.D.-T. was funded by Ministerio de Educacion y Ciencia, Spain, and by Marie Curie IEF (IEF-2008-237643). V.A.G. was supported by the Dorothy Hodgkin Fellowship. V.A.G. and A.F.M.M. were supported by the UK Biological and Biotechnology Research Council (BBSRC) via grant BB/J004553/1 to the John Innes Centre. I.B. was sponsored by an NWO VIDI grant. P.N.B. was funded by NIH grant R01-GM043778. L.B. was supported by Swedish Research Council and by Carl Tryggers Stiftelse grants. Work in James A.H. Murray laboratory was supported by the BBSRC grant BB/G00482X and by the ERASysBio+ initiative under the EU FP7 ERA-NET Plus scheme.

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2012.07.017

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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), 1002-1015. https://doi.org/10.1016/j.cell.2012.07.017

@article{2a6ea720a7634fb086574c9fbeb30a84,

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.",

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",

note = "Funding Information: We thank Dominique Bergmann for critically reviewing this manuscript; Fred Sack, Lieven de Veylder, Naohiro Kato, Dorus Gadella, Joachim Goedhart, Tom Beeckman, and Tom Bennett for materials; and Anah{\'i} P{\'e}rez-Torres, Luis Herrera-Estrella, and Juan Carlos del Pozo for technical advice. B.S. was supported by an ERC Advanced Investigator Fellowship and by ALW-ERAPG grant 855.50.017. A.C.-R. was supported by EMBO-ALTF 1114-2006 and CONACYT 000000000092916 grants. S.D.-T. was funded by Ministerio de Educacion y Ciencia, Spain, and by Marie Curie IEF (IEF-2008-237643). V.A.G. was supported by the Dorothy Hodgkin Fellowship. V.A.G. and A.F.M.M. were supported by the UK Biological and Biotechnology Research Council (BBSRC) via grant BB/J004553/1 to the John Innes Centre. I.B. was sponsored by an NWO VIDI grant. P.N.B. was funded by NIH grant R01-GM043778. L.B. was supported by Swedish Research Council and by Carl Tryggers Stiftelse grants. Work in James A.H. Murray laboratory was supported by the BBSRC grant BB/G00482X and by the ERASysBio+ initiative under the EU FP7 ERA-NET Plus scheme. ",

year = "2012",

month = aug,

day = "31",

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

language = "English (US)",

volume = "150",

pages = "1002--1015",

journal = "Cell",

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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. 1002-1015. 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

N1 - Funding Information: We thank Dominique Bergmann for critically reviewing this manuscript; Fred Sack, Lieven de Veylder, Naohiro Kato, Dorus Gadella, Joachim Goedhart, Tom Beeckman, and Tom Bennett for materials; and Anahí Pérez-Torres, Luis Herrera-Estrella, and Juan Carlos del Pozo for technical advice. B.S. was supported by an ERC Advanced Investigator Fellowship and by ALW-ERAPG grant 855.50.017. A.C.-R. was supported by EMBO-ALTF 1114-2006 and CONACYT 000000000092916 grants. S.D.-T. was funded by Ministerio de Educacion y Ciencia, Spain, and by Marie Curie IEF (IEF-2008-237643). V.A.G. was supported by the Dorothy Hodgkin Fellowship. V.A.G. and A.F.M.M. were supported by the UK Biological and Biotechnology Research Council (BBSRC) via grant BB/J004553/1 to the John Innes Centre. I.B. was sponsored by an NWO VIDI grant. P.N.B. was funded by NIH grant R01-GM043778. L.B. was supported by Swedish Research Council and by Carl Tryggers Stiftelse grants. Work in James A.H. Murray laboratory was supported by the BBSRC grant BB/G00482X and by the ERASysBio+ initiative under the EU FP7 ERA-NET Plus scheme.

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.

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U2 - 10.1016/j.cell.2012.07.017

DO - 10.1016/j.cell.2012.07.017

M3 - Article

C2 - 22921914

AN - SCOPUS:84865694816

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

Bibliographical note

ASJC Scopus subject areas

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