Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana
Abstract
Precise knowledge of spatial and temporal patterns of cell division, including number and orientation of divisions, and knowledge of cell expansion, is central to understanding morphogenesis. Our current knowledge of cell division patterns during plant and animal morphogenesis is largely deduced from analysis of clonal shapes and sizes. But such an analysis can reveal only the number, not the orientation or exact rate, of cell divisions. In this study, we have analyzed growth in real time by monitoring individual cell divisions in the shoot apical meristems (SAMs) of Arabidopsis thaliana. The live imaging technique has led to the development of a spatial and temporal map of cell division patterns. We have integrated cell behavior over time to visualize growth. Our analysis reveals temporal variation in mitotic activity and the cell division is coordinated across clonally distinct layers of cells. Temporal variation in mitotic activity is not correlated to the estimated plastochron length and diurnal rhythms. Cell division rates vary across the SAM surface. Cells in the peripheral zone (PZ) divide at a faster rate than in the central zone (CZ). Cell division rates in the CZ are relatively heterogeneous when compared with PZ cells. We have analyzed the cell behavior associated with flower primordium development starting from a stage at which the future flower comprises four cells in the L1 epidermal layer. Primordium development is a sequential process linked to distinct cellul…
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Boundaries are generally characterized by a low number of cell divisions and specific patterns of gene expression.
“In general, boundaries are characterized by a low number of cell divisions (Hussey, 1971;Reddy et al., 2004) and specific patterns of gene expression (Souer et al., 1996;Aida et al., 1997;Takada et al., 2001;Vroemen et al., 2003;Weir et al., 2004;Berger et al., 2009).”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Reddy et al., 2004
Boundary cells adopt a unique behavior encompassing infrequent cell divisions and limited cell expansion, leading to the establishment of a zone of reduced growth.
“All these data clearly suggest that boundary cells adopt a unique behavior, encompassing infrequent cell divisions and limited cell expansion, leading to the establishment of a zone of reduced growth (Reddy et al., 2004).”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Reddy et al., 2004
Cites
Floral dip: a simplified method for Agrobacterium ‐mediated transformation of Arabidopsis thaliana
Clough, S. J., & Bent, A. F. (1998) · The Plant Journal · doi:10.1046/j.1365-313x.1998.00343.x · Cited by 22,014 · see citing works
Multimodality image registration by maximization of mutual information
Maes, F., Collignon, A., Vandermeulen, D., Marchal, G., & Suetens, P. (1997) · IEEE Transactions on Medical Imaging · doi:10.1109/42.563664 · Cited by 4,547 · see citing works
Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation
Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., & Friml, J. (2003) · Cell · doi:10.1016/s0092-8674(03)00924-3 · Cited by 2,637 · see citing works
Early flower development in Arabidopsis.
Smyth, D. R., Bowman, J. L., & Meyerowitz, E. M. (1990) · The Plant Cell · doi:10.1105/tpc.2.8.755 · Cited by 2,155 · see citing works
Self-citationSchoof, H., Lenhard, M., Haecker, A., Mayer, K., Jürgens, G., & Laux, T. (2000) · Cell · doi:10.1016/s0092-8674(00)80700-x · Cited by 1,752 · see citing works
Role of WUSCHEL in Regulating Stem Cell Fate in the Arabidopsis Shoot Meristem
Mayer, K., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G., & Laux, T. (1998) · Cell · doi:10.1016/s0092-8674(00)81703-1 · Cited by 1,688 · see citing works
A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis
Long, J. A., Moan, E. I., Medford, J. I., & Barton, M. K. (1996) · Nature · doi:10.1038/379066a0 · Cited by 1,537 · see citing works
Regulation of phyllotaxis by polar auxin transport
Reinhardt, D., Pesce, E.-R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., & Kuhlemeier, C. (2003) · Nature · doi:10.1038/nature02081 · Cited by 1,523 · see citing works
Clark, S. E., Williams, R. W., & Meyerowitz, E. M. (1997) · Cell · doi:10.1016/s0092-8674(00)80239-1 · Cited by 1,373 · see citing works
Self-citationSignaling of Cell Fate Decisions by CLAVATA3 in Arabidopsis Shoot Meristems
Fletcher, J. C., Brand, U., Running, M., Simon, R. G., & Meyerowitz, E. M. (1999) · Science · doi:10.1126/science.283.5409.1911 · Cited by 1,359 · see citing works
Self-citationSteeves, T. A., & Sussex, I. M. (1989) · doi:10.1017/cbo9780511626227 · Cited by 1,334 · see citing works
The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis
Laux, T., Mayer, K., Berger, J., & Jürgens, G. (1996) · Development · doi:10.1242/dev.122.1.87 · Cited by 1,270 · see citing works
Dependence of Stem Cell Fate in Arabidopsis on a Feedback Loop Regulated by CLV3 Activity
Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M., & Simon, R. G. (2000) · Science · doi:10.1126/science.289.5479.617 · Cited by 1,123 · see citing works
Self-citationCutler, S. R., Ehrhardt, D. W., Griffitts, J. S., & Somerville, C. R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3718 · Cited by 988 · see citing works
Self-citationCLAVATA1, a regulator of meristem and flower development in Arabidopsis
Clark, S. E., Running, M., & Meyerowitz, E. M. (1993) · Development · doi:10.1242/dev.119.2.397 · Cited by 887 · see citing works
Self-citationAsymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis
Byrne, M. E., Barley, R., Curtis, M. D., Arroyo, J. M., Dunham, M. J., Hudson, A., & Martienssen, R. A. (2000) · Nature · doi:10.1038/35050091 · Cited by 816 · see citing works
Clark, S. E., Running, M., & Meyerowitz, E. M. (1995) · Development · doi:10.1242/dev.121.7.2057 · Cited by 735 · see citing works
Self-citationSpatio‐temporal analysis of mitotic activity with a labile cyclin–GUS fusion protein
Colón‐Carmona, A., You, R., Haimovitch‐Gal, T., & Doerner, P. W. (1999) · The Plant Journal · doi:10.1046/j.1365-313x.1999.00620.x · Cited by 659 · see citing works
Boisnard-Lorig, C., Colón‐Carmona, A., Bauch, M., Hodge, S., Doerner, P. W., Bancharel, E., Dumas, C., Haseloff, J. P., & Berger, F. (2001) · The Plant Cell · doi:10.1105/tpc.13.3.495 · Cited by 370 · see citing works
Genetic Control of Cell Division Patterns in Developing Plants
Meyerowitz, E. M. (1997) · Cell · doi:10.1016/s0092-8674(00)81868-1 · Cited by 368 · see citing works
Self-citationCLAVATA2, a regulator of meristem and organ development in Arabidopsis
Kayes, J. M., & Clark, S. E. (1998) · Development · doi:10.1242/dev.125.19.3843 · Cited by 356 · see citing works
Local expression of expansin induces the entire process of leaf development and modifies leaf shape
Pien, S., Wyrzykowska, J., McQueen‐Mason, S. J., Smart, C. C., & Fleming, A. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191380498 · Cited by 332 · see citing works
Regulation of CLV3 Expression by Two Homeobox Genes in Arabidopsis
Brand, U., Grünewald, M., Hobe, M., & Simon, R. G. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.001867 · Cited by 266 · see citing works
Cellular Parameters of the Shoot Apical Meristem in Arabidopsis
Laufs, P., Grandjean, O., Jonak, C., Kiêu, K., & Traas, J. A. (1998) · The Plant Cell · doi:10.1105/tpc.10.8.1375 · Cited by 248 · see citing works
Reinhardt, D., Wittwer, F., Mandel, T., & Kuhlemeier, C. J. (1998) · The Plant Cell · doi:10.1105/tpc.10.9.1427 · Cited by 230 · see citing works
Reinhardt, D., Frenz, M., Mandel, T., & Kuhlemeier, C. J. (2003) · Development · doi:10.1242/dev.00596 · Cited by 225 · see citing works
Grandjean, O., Vernoux, T., Laufs, P., Belcram, K., Mizukami, Y., & Traas, J. A. (2003) · The Plant Cell · doi:10.1105/tpc.017962 · Cited by 211 · see citing works
A fate map of the Arabidopsis embryonic shoot apical meristem
Irish, V. F., & Sussex, I. M. (1992) · Development · doi:10.1242/dev.115.3.745 · Cited by 205 · see citing works
Growth dynamics underlying petal shape and asymmetry
Rolland‐Lagan, A., Bangham, J., & Coen, E. (2003) · Nature · doi:10.1038/nature01443 · Cited by 195 · see citing works
The shoot apical meristem: its growth and development.
LYNDON, R. F. (1998) · Cambridge University Press eBooks · Cited by 134 · see citing works
Growth and morphogenesis at the vegetative shoot apex of Anagallis arvensis L.
Kwiatkowska, D. (2003) · Journal of Experimental Botany · doi:10.1093/jxb/erg166 · Cited by 133 · see citing works
Shapiro, B. E., Levchenko, A., Meyerowitz, E. M., Wold, B. J., & Mjolsness, E. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg042 · Cited by 122 · see citing works
Self-citationCell proliferation patterns in the wing imaginal disc of Drosophila
González‐Gaitán, M., Capdevila, M. P., & Garcı́a-Bellido, A. (1994) · Mechanisms of Development · doi:10.1016/0925-4773(94)90070-1 · Cited by 118 · see citing works
Analysis of surface growth in shoot apices
Dumais, J., & Kwiatkowska, D. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01350.x · Cited by 117 · see citing works
Initiation patterns of flower and floral organ development in Arabidopsis thaliana
Bossinger, G., & Smyth, D. R. (1996) · Development · doi:10.1242/dev.122.4.1093 · Cited by 111 · see citing works
Determining the role of patterned cell proliferation in the shape and size of the Drosophila wing
Resino, J., Salama‐Cohen, P., & Garcı́a-Bellido, A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.072208199 · Cited by 72 · see citing works
Surface growth at the reproductive shoot apex of Arabidopsis thaliana pin-formed 1 and wild type
Kwiatkowska, D. (2004) · Journal of Experimental Botany · doi:10.1093/jxb/erh109 · Cited by 69 · see citing works
Clonal analysis of leaf development in cotton
Dolan, L., & Poethig, R. S. (1998) · American Journal of Botany · doi:10.2307/2446322 · Cited by 47 · see citing works
Hern�ndez, L., Havelange, A., Bernier, G., & Green, P. (1991) · Planta · doi:10.1007/bf00194054 · Cited by 36 · see citing works
Cell division pattern influences gene expression in the shoot apical meristem
Wyrzykowska, J., & Fleming, A. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0930352100 · Cited by 34 · see citing works
Callos, J. D., DiRado, M., Xu, B., Behringer, F. J., Link, B. M., & Medford, J. I. (1994) · The Plant Journal · doi:10.1046/j.1365-313x.1994.6060835.x · Cited by 33 · see citing works
Cell fate in the inflorescence meristem and floral buttress of Arabidopsis thaliana
Furner, I. J., & Pumfrey, J. E. (1993) · The Plant Journal · doi:10.1046/j.1365-313x.1993.04060917.x · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Heisler, M. G., Ohno, C., Das, P., Sieber, P., Reddy, G. V., Long, J. A., & Meyerowitz, E. M. (2005) · Current Biology · doi:10.1016/j.cub.2005.09.052 · Cited by 1,189 · see citing works
Self-citationCoordination of carbon supply and plant growth
Smith, A. M., & Stitt, M. (2007) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2007.01708.x · Cited by 1,028 · see citing works
Pectin-Induced Changes in Cell Wall Mechanics Underlie Organ Initiation in Arabidopsis
Peaucelle, A., Braybrook, S. A., Guillou, L. L., Bron, É., Kuhlemeier, C. J., & Höfte, H. (2011) · Current Biology · doi:10.1016/j.cub.2011.08.057 · Cited by 627 · see citing works
WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apexPreprint
Yadav, R. K., Perales, M., Gruel, J., Girke, T., Jönsson, H., & Reddy, G. V. (2011) · Genes & Development · doi:10.1101/gad.17258511 · Cited by 622 · see citing works
Self-citationMorphoGraphX: A platform for quantifying morphogenesis in 4D
de Reuille, P. B., Routier‐Kierzkowska, A., Kierzkowski, D., Bassel, G. W., Schuepbach, T., Tauriello, G., Bajpai, N., Strauss, S., Weber, A. R., Kiss, A., et al. (2015) · eLife · doi:10.7554/elife.05864 · Cited by 542 · see citing works
A Polycomb-based switch underlying quantitative epigenetic memory
Angel, A., Song, J., Dean, C., & Howard, M. (2011) · Nature · doi:10.1038/nature10241 · Cited by 478 · see citing works
Heisler, M. G., Hamant, O., Krupinski, P., Uyttewaal, M., Ohno, C., Jönsson, H., Traas, J., & Meyerowitz, E. M. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000516 · Cited by 459 · see citing works
Self-citationSlicing across Kingdoms: Regeneration in Plants and Animals
Birnbaum, K. D., & Alvarado, A. S. (2008) · Cell · doi:10.1016/j.cell.2008.01.040 · Cited by 424 · see citing works
Agriculture and the new challenges for photosynthesis research
Murchie, E. H., Pinto, M. E., & Horton, P. (2008) · New Phytologist · doi:10.1111/j.1469-8137.2008.02705.x · Cited by 395 · see citing works
Pattern formation during de novo assembly of the Arabidopsis shoot meristem
Gordon, S., Heisler, M. G., Reddy, G. V., Ohno, C. K., Das, P. K., & Meyerowitz, E. M. (2007) · Development · doi:10.1242/dev.010298 · Cited by 387 · see citing works
Self-citationTwenty years on: The inner workings of the shoot apical meristem, a developmental dynamo
Barton, M. K. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2009.11.029 · Cited by 372 · see citing works
Etchells, J. P., & Turner, S. R. (2010) · Development · doi:10.1242/dev.044941 · Cited by 363 · see citing works
Stem-cell niches: nursery rhymes across kingdoms
Scheres, B. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2164 · Cited by 355 · see citing works
Cell to whole-plant phenotyping: the best is yet to come
Dhondt, S., Wuyts, N., & Inzé, D. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.04.008 · Cited by 348 · see citing works
Sieber, P., Wellmer, F., Gheyselinck, J., Riechmann, J. L., & Meyerowitz, E. M. (2007) · Development · doi:10.1242/dev.02817 · Cited by 346 · see citing works
Self-citationThe Orientation of Cell Divisions Determines the Shape of Drosophila Organs
Baena-López, L. A., Baonza, A., & Garcı́a-Bellido, A. (2005) · Current Biology · doi:10.1016/j.cub.2005.07.062 · Cited by 332 · see citing works
Arabidopsis TCP20 links regulation of growth and cell division control pathways
Li, C., Potuschak, T., Colón‐Carmona, A., Gutiérrez, R. A., & Doerner, P. W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504039102 · Cited by 327 · see citing works
Alvarez-Buylla, E. R., Benítez, M., Corvera-Poiré, A., Chaos, Á., de Folter, S., Buen, A. G.-D., Garay‐Arroyo, A., García‐Ponce, B., Jaimes‐Miranda, F., Pérez-Ruíz, R. V., et al. (2010) · The Arabidopsis Book · doi:10.1199/tab.0127 · Cited by 313 · see citing works
Elastic Domains Regulate Growth and Organogenesis in the Plant Shoot Apical Meristem
Kierzkowski, D., Nakayama, N., Routier‐Kierzkowska, A., Weber, A. R., Bayer, E., Schorderet, M., Reinhardt, D., Kuhlemeier, C. J., & Smith, R. S. (2012) · Science · doi:10.1126/science.1213100 · Cited by 303 · see citing works
Roeder, A., Chickarmane, V. S., Cunha, A., Obara, B., Manjunath, B. S., & Meyerowitz, E. M. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000367 · Cited by 301 · see citing works
Self-citationImaging plant growth in 4D: robust tissue reconstruction and lineaging at cell resolution
Fernandez, R., Das, P. K., Mirabet, V., Moscardi, E., Traas, J. A., Verdeil, J., Malandain, G., & Godin, C. (2010) · Nature Methods · doi:10.1038/nmeth.1472 · Cited by 299 · see citing works
A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristemPreprint
Sun, B., Xu, Y., Ng, K.-H., & Ito, T. (2009) · Genes & Development · doi:10.1101/gad.1800409 · Cited by 298 · see citing works
Rethinking Differentiation: Stem Cells, Regeneration, and Plasticity
Alvarado, A. S., & Yamanaka, S. (2014) · Cell · doi:10.1016/j.cell.2014.02.041 · Cited by 272 · see citing works
Redox regulation of plant stem cell fate
Zeng, J., Dong, Z., Wu, H., Tian, Z., & Zhao, Z. (2017) · The EMBO Journal · doi:10.15252/embj.201695955 · Cited by 269 · see citing works
Stem-Cell Homeostasis and Growth Dynamics Can Be Uncoupled in the Arabidopsis Shoot Apex
Reddy, G. V., & Meyerowitz, E. M. (2005) · Science · doi:10.1126/science.1116261 · Cited by 259 · see citing works
Self-citationMegason, S. G., & Fraser, S. E. (2007) · Cell · doi:10.1016/j.cell.2007.08.031 · Cited by 250 · see citing works
The flowering of Arabidopsis flower development
Irish, V. F. (2009) · The Plant Journal · doi:10.1111/j.1365-313x.2009.04065.x · Cited by 247 · see citing works
Using movies to analyse gene circuit dynamics in single cells
Locke, J. C. W., & Elowitz, M. B. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2056 · Cited by 238 · see citing works
Orchestrating size and shape during morphogenesis
Lecuit, T., & LeGoff, L. (2007) · Nature · doi:10.1038/nature06304 · Cited by 230 · see citing works
Cytokinin Signaling Activates WUSCHEL Expression during Axillary Meristem Initiation
Wang, J., Tian, C., Zhang, C., Shi, B., Cao, X., Zhang, T.-Q., Zhao, Z., Wang, J., & Jiao, Y. (2017) · The Plant Cell · doi:10.1105/tpc.16.00579 · Cited by 228 · see citing works
Vernalization – a cold-induced epigenetic switch
Song, J., Angel, A., Howard, M., & Dean, C. (2012) · Journal of Cell Science · doi:10.1242/jcs.084764 · Cited by 226 · see citing works
Soybean Sowing Date: The Vegetative, Reproductive, and Agronomic Impacts
Bastidas, A., Setiyono, T., Dobermann, A., Cassman, K. G., Elmore, R. W., Graef, G. L., & Specht, J. E. (2008) · Crop Science · doi:10.2135/cropsci2006.05.0292 · Cited by 226 · see citing works
The never-ending story: from pluripotency to plant developmental plasticity
Gaillochet, C., & Lohmann, J. U. (2015) · Development · doi:10.1242/dev.117614 · Cited by 223 · see citing works
The mechanics behind plant development
Hamant, O., & Traas, J. A. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2009.03100.x · Cited by 222 · see citing works
Distinct phases of Polycomb silencing to hold epigenetic memory of cold in Arabidopsis
Yang, H., Berry, S., Olsson, T. S. G., Hartley, M., Howard, M., & Dean, C. (2017) · Science · doi:10.1126/science.aan1121 · Cited by 220 · see citing works
Molecular mechanism of cytokinin-activated cell division in Arabidopsis
Yang, W., Cortijo, S., Korsbo, N., Roszak, P., Schiessl, K., Gurzadyan, A. V., Wightman, R., Jönsson, H., & Meyerowitz, E. M. (2021) · Science · doi:10.1126/science.abe2305 · Cited by 205 · see citing works
Self-citationTiming Mechanism Dependent on Cell Division Is Invoked by Polycomb Eviction in Plant Stem Cells
Sun, B., Looi, L., Guo, S., He, Z., Gan, E., Huang, J., Xu, Y., Wee, W.-Y., & Ito, T. (2014) · Science · doi:10.1126/science.1248559 · Cited by 204 · see citing works
Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche
Willis, L., Refahi, Y., Wightman, R., Landrein, B., Teles, J., Huang, K. C., Meyerowitz, E. M., & Jönsson, H. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616768113 · Cited by 198 · see citing works
Self-citationStoma, S., Lucas, M., Chopard, J., Schaedel, M., Traas, J. A., & Godin, C. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000207 · Cited by 197 · see citing works
Suzaki, T., Yano, K., Ito, M., Umehara, Y., Suganuma, N., & Kawaguchi, M. (2012) · Development · doi:10.1242/dev.084079 · Cited by 193 · see citing works
DNA replication–coupled histone modification maintains Polycomb gene silencing in plants
Jiang, D., & Berger, F. (2017) · Science · doi:10.1126/science.aan4965 · Cited by 190 · see citing works
Prasad, K., Parameswaran, S., & Vijayraghavan, U. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02504.x · Cited by 188 · see citing works
The Role of Mechanical Forces in Plant Morphogenesis
Mirabet, V., Das, P. K., Boudaoud, A., & Hamant, O. (2011) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042110-103852 · Cited by 186 · see citing works
HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers
Zhou, Y., Yan, A., Han, H., Li, T., Geng, Y., Liu, X., & Meyerowitz, E. M. (2018) · Science · doi:10.1126/science.aar8638 · Cited by 178 · see citing works
Self-citationComputational models of plant development and form
Prusinkiewicz, P., & Runions, A. (2012) · New Phytologist · doi:10.1111/j.1469-8137.2011.04009.x · Cited by 173 · see citing works
Maizel, A., von Wangenheim, D., Federici, F., Haseloff, J. P., & Stelzer, E. H. K. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04692.x · Cited by 167 · see citing works
Landrein, B., Kiss, A., Sassi, M., Chauvet, A., Das, P., Cortizo, M., Laufs, P., Takeda, S., Aida, M., Traas, J., et al. (2015) · eLife · doi:10.7554/elife.07811 · Cited by 167 · see citing works
Stem cell activation by light guides plant organogenesisPreprint
Yoshida, S., Mandel, T., & Kuhlemeier, C. J. (2011) · Genes & Development · doi:10.1101/gad.631211 · Cited by 165 · see citing works
Threshold-dependent transcriptional discrimination underlies stem cell homeostasis
Perales, M., Rodriguez, K., Snipes, S. A., Yadav, R. K., Díaz‐Mendoza, M., & Reddy, G. V. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1607669113 · Cited by 163 · see citing works
Self-citationQuantitative Time-Lapse Fluorescence Microscopy in Single Cells
Muzzey, D., & van Oudenaarden, A. (2009) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.042308.113408 · Cited by 157 · see citing works
Flowering and apical meristem growth dynamics
Kwiatkowska, D. (2008) · Journal of Experimental Botany · doi:10.1093/jxb/erm290 · Cited by 156 · see citing works
Genetic control of shoot organ boundaries
Aida, M., & Tasaka, M. (2005) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2005.11.011 · Cited by 155 · see citing works
Physical Forces Regulate Plant Development and Morphogenesis
Sampathkumar, A., Yan, A., Krupinski, P., & Meyerowitz, E. M. (2014) · Current Biology · doi:10.1016/j.cub.2014.03.014 · Cited by 155 · see citing works
Self-citationThe <i>Arabidopsis</i> genome: A foundation for plant research
Bevan, M., & Walsh, S. (2005) · Genome Research · doi:10.1101/gr.3723405 · Cited by 153 · see citing works
Histone modifications and their regulatory roles in plant development and environmental memory
Zhao, T., Zhan, Z., & Jiang, D. (2019) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2019.09.005 · Cited by 152 · see citing works
Two-Step Regulation of a Meristematic Cell Population Acting in Shoot Branching in Arabidopsis
Shi, B., Zhang, C., Tian, C., Wang, J., Wang, Q., Xu, T., Xu, Y., Ohno, C., Sablowski, R., Heisler, M. G., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006168 · Cited by 150 · see citing works
“In addition, we also used reporter lines to follow expression of the shoot meristem central zone stem cell marker CLAVATA3 (CLV3), the shoot meristem organizing center marker WUSCHEL (WUS), and the pericycle-like cell marker J0121, which marks progenitor cells for regeneration [3, 32, 33].”
MethodSelf-citationTracing Cells for Tracking Cell Lineage and Clonal Behavior
BUCKINGHAM, M. E., & Meilhac, S. M. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.07.019 · Cited by 149 · see citing works
Arabidopsis PLETHORA Transcription Factors Control Phyllotaxis
Prasad, K., Grigg, S. P., Barkoulas, M., Yadav, R. K., Sanchez‐Perez, G. F., Pinon, V., Blilou, I., Hofhuis, H. F., Dhonukshe, P., Galinha, C., et al. (2011) · Current Biology · doi:10.1016/j.cub.2011.05.009 · Cited by 148 · see citing works
Self-citationKuhlemeier, C. J. (2007) · Trends in Plant Science · doi:10.1016/j.tplants.2007.03.004 · Cited by 146 · see citing works
Jones, A. R., Forero, M. G., Withers, S. P., Smith, R. S., Traas, J. A., Dewitte, W., & Murray, J. A. H. (2017) · Nature Communications · doi:10.1038/ncomms15060 · Cited by 145 · see citing works
Stem cell regulation in the Arabidopsis shoot apical meristem
Williams, L. E., & Fletcher, J. C. (2005) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2005.09.010 · Cited by 145 · see citing works
From genes to shape: regulatory interactions in leaf development
Barkoulas, M., Galinha, C., Grigg, S. P., & Tsiantis, M. (2007) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2007.07.012 · Cited by 144 · see citing works
Braybrook, S. A., & Kuhlemeier, C. J. (2010) · The Plant Cell · doi:10.1105/tpc.110.073924 · Cited by 142 · see citing works
Modeling the organization of the WUSCHEL expression domain in the shoot apical meristem
Jönsson, H., Heisler, M. G., Reddy, G. V., Agrawal, V., Gor, V., Shapiro, B. E., Mjolsness, E., & Meyerowitz, E. M. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti1036 · Cited by 140 · see citing works
Self-citationYadav, R. K., Tavakkoli, M., & Reddy, G. V. (2010) · Development · doi:10.1242/dev.054973 · Cited by 137 · see citing works
Self-citationZeng, G., Taylor, S. M., McColm, J. R., Kappas, N. C., Kearney, J. B., Williams, L. H., Hartnett, M. E., & Bautch, V. L. (2006) · Blood · doi:10.1182/blood-2006-07-037952 · Cited by 136 · see citing works
Plant Stem Cell Signaling Involves Ligand-Dependent Trafficking of the CLAVATA1 Receptor Kinase
Nimchuk, Z. L., Tarr, P. T., Ohno, C. K., Qu, X., & Meyerowitz, E. M. (2011) · Current Biology · doi:10.1016/j.cub.2011.01.039 · Cited by 135 · see citing works
Self-citationDo plants have a segregated germline?
Lanfear, R. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2005439 · Cited by 133 · see citing works
Time‐lapse analysis of stem‐cell divisions in the Arabidopsis thaliana root meristem
Campilho, A., Garcia, B., van den Toorn, H., Wijk, H. V., Campilho, A., & Scheres, B. (2006) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02892.x · Cited by 127 · see citing works
A high-resolution gene expression map of the Arabidopsis shoot meristem stem cell niche
Yadav, R. K., Tavakkoli, M., Xie, M., Girke, T., & Reddy, G. V. (2014) · Development · doi:10.1242/dev.106104 · Cited by 126 · see citing works
Self-citationRay, R. P., Matamoro‐Vidal, A., Ribeiro, P. S., Tapon, N., Houle, D., Salazar‐Ciudad, I., & Thompson, B. J. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.06.019 · Cited by 124 · see citing works
Patterning and Polarity in Seed Plant Shoots
Bowman, J. L., & Floyd, S. K. (2007) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.57.032905.105356 · Cited by 124 · see citing works
Systems Approaches to Identifying Gene Regulatory Networks in Plants
Long, T. A., Brady, S. M., & Benfey, P. N. (2008) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.24.110707.175408 · Cited by 122 · see citing works
Mechanisms Underlying the Environmentally Induced Plasticity of Leaf Morphology
Fritz, M. A., Rosa, S., & Sicard, A. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00478 · Cited by 119 · see citing works
Shoot Apical Meristem Form and Function
Ha, C. M., Jun, J. H., & Fletcher, J. C. (2010) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(10)91004-1 · Cited by 119 · see citing works
Temperature-dependent growth contributes to long-term cold sensing
Zhao, Y., Antoniou-Kourounioti, R. L., Calder, G. M., Dean, C., & Howard, M. (2020) · Nature · doi:10.1038/s41586-020-2485-4 · Cited by 116 · see citing works
The Arabidopsis petal: a model for plant organogenesis
Irish, V. F. (2008) · Trends in Plant Science · doi:10.1016/j.tplants.2008.05.006 · Cited by 113 · see citing works
Morphogenesis and Patterning at the Organ Boundaries in the Higher Plant Shoot Apex
Aida, M., & Tasaka, M. (2006) · Plant Molecular Biology · doi:10.1007/s11103-005-2760-7 · Cited by 113 · see citing works
The Hormonal Control of Regeneration in Plants
Su, Y. H., & Zhang, X. S. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-391498-9.00010-3 · Cited by 109 · see citing works
<i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems
Wang, Q., Hasson, A., Rossmann, S., & Theres, K. (2016) · New Phytologist · doi:10.1111/nph.13641 · Cited by 106 · see citing works
QUANTITATIVE FLUORESCENCE MICROSCOPY: From Art to Science
Fricker, M. D., Runions, J., & Moore, I. R. (2006) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.57.032905.105239 · Cited by 105 · see citing works
A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem
Dodsworth, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.09.031 · Cited by 103 · see citing works
Control of Tissue and Organ Growth in Plants
Breuninger, H., & Lenhard, M. (2010) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(10)91007-7 · Cited by 100 · see citing works
Watson, J. M., Platzer, A., Kazda, A., Akimcheva, S., Valuchova, S. B., Nizhynska, V., Nordborg, M., & Říha, K. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1609686113 · Cited by 98 · see citing works
From genes to networks: The genetic control of leaf development
Wang, H., Kong, F., & Zhou, C. (2021) · Journal of Integrative Plant Biology · doi:10.1111/jipb.13084 · Cited by 98 · see citing works
Towards the systems biology of auxin-transport-mediated patterning
Berleth, T., Scarpella, E., & Prusinkiewicz, P. (2007) · Trends in Plant Science · doi:10.1016/j.tplants.2007.03.005 · Cited by 98 · see citing works
Live cell imaging of meiosis in Arabidopsis thaliana
Prusicki, M. A., Keizer, E. M., van Rosmalen, R. P., Komaki, S., Seifert, F., Müller, K., Wijnker, T. G., Fleck, C. C., & Schnittger, A. (2019) · eLife · doi:10.7554/elife.42834 · Cited by 97 · see citing works
From primary to secondary growth: origin and development of the vascular system
Baucher, M., Jaziri, M. E., & Vandeputte, O. M. (2007) · Journal of Experimental Botany · doi:10.1093/jxb/erm185 · Cited by 97 · see citing works
Schlegel, J., Denay, G., Wink, R. H., Pinto, K. G., Stahl, Y., Schmid, J., Blümke, P., & Simon, R. G. (2021) · eLife · doi:10.7554/elife.70934 · Cited by 94 · see citing works
Cheng, X., Peng, J., Ma, J., Tang, Y., Chen, R., Mysore, K. S., & Wen, J. (2012) · New Phytologist · doi:10.1111/j.1469-8137.2012.04147.x · Cited by 93 · see citing works
O Cell, Where Art Thou? The mechanisms of shoot meristem patterning
Gaillochet, C., Daum, G., & Lohmann, J. U. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2014.11.002 · Cited by 92 · see citing works
Kwiatkowska, D. (2005) · Journal of Experimental Botany · doi:10.1093/jxb/erj042 · Cited by 92 · see citing works
Cho, E., & Zambryski, P. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018542108 · Cited by 91 · see citing works
The developmental context of cell-cycle control in plants
de Jager, S. M., Maughan, S. C., Dewitte, W., Scofield, S., & Murray, J. A. H. (2005) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2005.02.004 · Cited by 90 · see citing works
Stress and Strain Provide Positional and Directional Cues in Development
Bozorg, B., Krupinski, P., & Jönsson, H. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003410 · Cited by 87 · see citing works
Meng, L., & Feldman, L. J. (2010) · Planta · doi:10.1007/s00425-010-1236-4 · Cited by 86 · see citing works
Hormone mediated regulation of the shoot apical meristem
Veit, B. E. (2008) · Plant Molecular Biology · doi:10.1007/s11103-008-9396-3 · Cited by 85 · see citing works
Regulation of floral stem cell termination in Arabidopsis
Sun, B., & Ito, T. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00017 · Cited by 85 · see citing works
Jenik, P. D., Jurkuta, R. E. J., & Barton, M. K. (2005) · The Plant Cell · doi:10.1105/tpc.105.036889 · Cited by 85 · see citing works
Time‐lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation
Sawchuk, M. G., Head, P., Donner, T. J., & Scarpella, E. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2007.02193.x · Cited by 84 · see citing works
- Authors
- Reddy, G. V., Heisler, M. G., Ehrhardt, D. W., & Meyerowitz, E. M.
- Affiliations
- California Institute of Technology (US)
- Carnegie Institution for Science (US)
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2004-09-01
- Volume
- 131
- Issue
- 17
- Pages
- 4225-4237
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2151319306
- Cited by
- 339
- References
- 42
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 8 · 2023: 13 · 2022: 8 · 2021: 20 · 2020: 10 · 2019: 14 · 2018: 17 · 2017: 22 · 2016: 15 · 2015: 11 · 2014: 19 · 2013: 15 · 2012: 15
- FWCI
- 23.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant tissue culture and regeneration
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- oriented cell division, shoot apical meristem, morphogenesis, cell division rate, cell expansion, live-cell imaging, Arabidopsis thaliana, peripheral zone, central zone, mitotic activity, plastochron, diurnal cycle, clonal analysis, flower bud formation
- MeSH terms
- Bacterial Proteins, Cell Cycle, Cell Division, Fluorescent Dyes, Image Processing, Computer-Assisted, Luminescent Proteins, Mitosis, Plant Proteins, Plasmids, Stem Cells, Time Factors, Arabidopsis, Gene Expression Regulation, Plant, Plant Shoots, Cell Lineage, Transgenes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review