A Bistable Circuit Involving SCARECROW-RETINOBLASTOMA Integrates Cues to Inform Asymmetric Stem Cell Division

被引:274
作者
Cruz-Ramirez, Alfredo [2 ]
Diaz-Trivino, Sara [2 ]
Blilou, Ikram [2 ]
Grieneisen, Veronica A. [1 ,3 ]
Sozzani, Rosangela [4 ,5 ]
Zamioudis, Christos [2 ]
Miskolczi, Pal [6 ,7 ]
Nieuwland, Jeroen [8 ]
Benjamins, Rene [2 ]
Dhonukshe, Pankaj [2 ]
Caballero-Perez, Juan [9 ]
Horvath, Beatrix [2 ]
Long, Yuchen [2 ]
Mahonen, Ari Pekka [2 ]
Zhang, Hongtao [2 ]
Xu, Jian [2 ]
Murray, James A. H. [8 ]
Benfey, Philip N. [4 ,5 ]
Bako, Laszlo [6 ,7 ]
Maree, Athanasius F. M. [1 ]
Scheres, Ben [2 ]
机构
[1] John Innes Ctr, Dept Computat & Syst Biol, Norwich NR4 7UH, Norfolk, England
[2] Univ Utrecht, Dept Biol, NL-3584 CH Utrecht, Netherlands
[3] Univ E Anglia, Sch Biol Sci, Dept Cell & Dev Biol, Norwich NR4 7TJ, Norfolk, England
[4] Duke Univ, Dept Biol, Ctr Syst Biol, Durham, NC 27708 USA
[5] Duke Univ, Inst Genome Sci & Policy, Ctr Syst Biol, Durham, NC 27708 USA
[6] Umea Univ, Dept Plant Physiol, Umea Plant Sci Ctr, S-90187 Umea, Sweden
[7] Swedish Univ Agr Sci, Dept Forest Genet & Plant Physiol, Umea Plant Sci Ctr, S-90183 Umea, Sweden
[8] Cardiff Sch Biosci, Cardiff CF10 3AX, S Glam, Wales
[9] Inst Syst Biol, Seattle, WA 98109 USA
基金
瑞典研究理事会; 英国生物技术与生命科学研究理事会;
关键词
PROTEIN-PROTEIN INTERACTIONS; ARABIDOPSIS ROOT-MERISTEM; TUMOR-SUPPRESSOR; SPLIT LUCIFERASE; AUXIN TRANSPORT; CYCLE; GENE; DIFFERENTIATION; PLANTS; GROWTH;
D O I
10.1016/j.cell.2012.07.017
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
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 RETINOBLASTOM-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.
引用
收藏
页码:1002 / 1015
页数:14
相关论文
共 52 条
[1]   Asymmetric Cell Divisions: A View from Plant Development [J].
Abrash, Emily B. ;
Bergmann, Dominique C. .
DEVELOPMENTAL CELL, 2009, 16 (06) :783-796
[2]   Network motifs: theory and experimental approaches [J].
Alon, Uri .
NATURE REVIEWS GENETICS, 2007, 8 (06) :450-461
[3]   The retinoblastoma protein tumor suppressor is important for appropriate osteoblast differentiation and bone development [J].
Berman, Seth D. ;
Yuan, Tina L. ;
Miller, Emily S. ;
Lee, Eunice Y. ;
Caron, Alicia ;
Lees, Jacqueline A. .
MOLECULAR CANCER RESEARCH, 2008, 6 (09) :1440-1451
[4]   A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex [J].
Boniotti, MB ;
Gutierrez, C .
PLANT JOURNAL, 2001, 28 (03) :341-350
[5]   Arabidopsis RETINOBLASTOMA-RELATED Is Required for Stem Cell Maintenance, Cell Differentiation, and Lateral Organ Production [J].
Borghi, Lorenzo ;
Gutzat, Ruben ;
Fuetterer, Johannes ;
Laizet, Yec'han ;
Hennig, Lars ;
Gruissem, Wilhelm .
PLANT CELL, 2010, 22 (06) :1792-1811
[6]   Functional Modules in the Arabidopsis Core Cell Cycle Binary Protein-Protein Interaction Network [J].
Boruc, Joanna ;
Van den Daele, Hilde ;
Hollunder, Jens ;
Rombauts, Stephane ;
Mylle, Evelien ;
Hilson, Pierre ;
Inze, Dirk ;
De Veylder, Lieven ;
Russinova, Eugenia .
PLANT CELL, 2010, 22 (04) :1264-1280
[7]   Rb regulates fate choice and lineage commitment in vivo [J].
Calo, Eliezer ;
Quintero-Estades, Jose A. ;
Danielian, Paul S. ;
Nedelcu, Simona ;
Berman, Seth D. ;
Lees, Jacqueline A. .
NATURE, 2010, 466 (7310) :1110-U126
[8]   Rb-mediated neuronal differentiation through cell-cycle-independent regulation of E2f3a [J].
Chen, Danian ;
Opavsky, Rene ;
Pacal, Marek ;
Tanimoto, Naoyuki ;
Wenzel, Pamela ;
Seeliger, Mathias W. ;
Leone, Gustavo ;
Bremner, Rod .
PLOS BIOLOGY, 2007, 5 (07) :1504-1519
[9]   Firefly luciferase complementation imaging assay for protein-protein interactions in plants [J].
Chen, Huamin ;
Zou, Yan ;
Shang, Yulei ;
Lin, Huiqiong ;
Wang, Yujing ;
Cai, Run ;
Tang, Xiaoyan ;
Zhou, Jian-Min .
PLANT PHYSIOLOGY, 2008, 146 (02) :368-376
[10]   Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs [J].
Chen, PL ;
Riley, DJ ;
Chen, YM ;
Lee, WH .
GENES & DEVELOPMENT, 1996, 10 (21) :2794-2804