How boundaries control plant development
Abstract
Continuous growth and organ development from the shoot apical meristem (SAM) requires a precise coordination of stem cell proliferation, commitment of stem cell descendants to diverse differentiation pathways and establishment of morphological meristem-to-organ boundaries. These complex biological processes require extensive integration of several components of cell-to-cell signaling and gene regulatory networks whose coordinated actions have an impact on cell division and growth. Here we review the current knowledge of gene networks involved in organogenesis from the SAM in higher plants. We focus on recent advances to show how the interaction between transcriptional regulators, hormonal crosstalk and physical stress regulates the establishment and maintenance of meristem-to-organ boundaries. Continuous growth and organ development from the shoot apical meristem (SAM) requires a precise coordination of stem cell proliferation, commitment of stem cell descendants to diverse differentiation pathways and establishment of morphological meristem-to-organ boundaries. These complex biological processes require extensive integration of several components of cell-to-cell signaling and gene regulatory networks whose coordinated actions have an impact on cell division and growth. Here we review the current knowledge of gene networks involved in organogenesis from the SAM in higher plants. We focus on recent advances to show how the interaction between transcriptional regulators, hormonal crosstalk and physical stress regulates the establishment and maintenance of meristem-to-organ boundaries.
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The boundary zone fulfills an important function in meristem maintenance and organ development.
“This zone is not just a border but fulfills an important function in meristem maintenance and organ development (Zadnikova and Simon, 2014).”
From Shaping plant architecture (2015) · cites this paper as Zadnikova and Simon, 2014
Cites
Uyttewaal, M., Burian, A., Alim, K., Landrein, B., Borowska-Wykręt, D., Berne-Dedieu, A., Peaucelle, A., Ludynia, M., Traas, J. A., Boudaoud, A., et al. (2012) · Cell · doi:10.1016/j.cell.2012.02.048 · Cited by 481 · see citing works
Model for the regulation of <i>Arabidopsis thaliana</i> leaf margin development
Bilsborough, G. D., Runions, A., Barkoulas, M., Jenkins, H. W., Hasson, A., Galinha, C., Laufs, P., Hay, A., Prusinkiewicz, P., & Tsiantis, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015162108 · Cited by 467 · 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
Koyama, T., Mitsuda, N., Seki, M., Shinozaki, K., & Ohme‐Takagi, M. (2010) · The Plant Cell · doi:10.1105/tpc.110.075598 · Cited by 417 · see citing works
Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes
Li, S., Lei, L., Somerville, C. R., & Gu, Y. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118560109 · Cited by 331 · see citing works
Tabuchi, H., Zhang, Y., Hattori, S., Omae, M., Shimizu‐Sato, S., Oikawa, T., Qian, Q., Nishimura, M., Kitano, H., Xie, H., et al. (2011) · The Plant Cell · doi:10.1105/tpc.111.088765 · Cited by 270 · see citing works
Two-Step Regulation of LAX PANICLE1 Protein Accumulation in Axillary Meristem Formation in Rice
Oikawa, T., & Kyozuka, J. (2009) · The Plant Cell · doi:10.1105/tpc.108.065425 · Cited by 251 · see citing works
Chuck, G. S., Whipple, C., Jackson, D. P., & Hake, S. (2010) · Development · doi:10.1242/dev.048348 · Cited by 246 · see citing works
Berckmans, B., Vassileva, V., Schmid, S. P. C., Maes, S., Parizot, B., Naramoto, S., Magyar, Z., Kamei, C. L. A., Koncz, C., Bögre, L., et al. (2011) · The Plant Cell · doi:10.1105/tpc.111.088377 · Cited by 239 · see citing works
Self-citationMilani, P., Gholamirad, M., Traas, J. A., Arnéodo, A., Boudaoud, A., Argoul, F., & Hamant, O. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04649.x · Cited by 231 · see citing works
Gendron, J. M., Liu, J.-S., Fan, M., Bai, M.-Y., Wenkel, S., Springer, P. S., Barton, M. K., & Wang, Z.-Y. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210799110 · Cited by 205 · see citing works
Bell, E. M., Lin, W.-C., Husbands, A. Y., Yu, L., Jaganatha, V., Jablonska, B., Mangeon, A., Neff, M. M., Girke, T., & Springer, P. S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210789109 · Cited by 194 · see citing works
Plant development: A TALE story
Hamant, O., & Pautot, V. (2010) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2010.01.015 · Cited by 192 · see citing works
Auxin at the Shoot Apical MeristemPreprint
Vernoux, T., Besnard, F., & Traas, J. A. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001487 · Cited by 183 · see citing works
Lodha, M., Marco, C. F., & Timmermans, M. C. P. (2013) · Genes & Development · doi:10.1101/gad.211425.112 · Cited by 175 · see citing works
Lee, D.-K., Geisler, M., & Springer, P. S. (2009) · Development · doi:10.1242/dev.031971 · Cited by 164 · see citing works
Nakano, T., Kimbara, J., Fujisawa, M., Kitagawa, M., Ihashi, N., Maeda, H., Kasumi, T., & Ito, Y. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.183731 · Cited by 162 · see citing works
Shi, C., Stenvik, G., Vie, A. K., Bones, A. M., Pautot, V., Proveniers, M. C. G., Aalen, R. B., & Butenko, M. A. (2011) · The Plant Cell · doi:10.1105/tpc.111.084608 · Cited by 160 · see citing works
Takeda, S., Hanano, K., Kariya, A., Shimizu, S., Zhao, L., Matsui, M., Tasaka, M., & Aida, M. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04571.x · Cited by 146 · see citing works
Jun, J. H., Ha, C. M., & Fletcher, J. C. (2010) · The Plant Cell · doi:10.1105/tpc.109.070763 · Cited by 145 · see citing works
A Mechanistic Link between<i>STM</i>and<i>CUC1</i>during Arabidopsis Development
Spinelli, S. V., Martin, A. P., Viola, I. L., Gonzalez, D. H., & Palatnik, J. F. (2011) · Plant Physiology · doi:10.1104/pp.111.177709 · Cited by 145 · see citing works
Yordanov, Y. S., Regan, S., & Busov, V. B. (2010) · The Plant Cell · doi:10.1105/tpc.110.078634 · Cited by 140 · see citing works
JAGGED Controls Arabidopsis Petal Growth and Shape by Interacting with a Divergent Polarity Field
Sauret-Gueto, S., Schiessl, K., Bangham, A., Sablowski, R. W. M., & Coen, E. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001550 · Cited by 137 · see citing works
Crowell, E. F., Timpano, H., Desprez, T., Franssen-Verheijen, T., Emons, A. C., Höfte, H., & Vernhettes, S. (2011) · The Plant Cell · doi:10.1105/tpc.111.087338 · Cited by 130 · see citing works
Uberti‐Manassero, N. G., Lucero, L. E., Viola, I. L., Vegetti, A. C., & González, D. H. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err305 · Cited by 113 · see citing works
Auxin controls petal initiation in Arabidopsis
Lampugnani, E. R., Kilinc, A., & Smyth, D. R. (2012) · Development · doi:10.1242/dev.084582 · Cited by 109 · see citing works
Early inflorescence development in the grasses (Poaceae)
Kellogg, E. A., Câmara, P. E. A. S., Rudall, P. J., Ladd, P. G., Malcomber, S. T., Whipple, C., & Doust, A. N. (2013) · Frontiers in Plant Science · doi:10.3389/fpls.2013.00250 · Cited by 100 · see citing works
Ikezaki, M., Kojima, M., Sakakibara, H., Kojima, S., Ueno, Y., Machida, C., & Machida, Y. (2010) · The Plant Journal · doi:10.1111/j.1365-313x.2009.04033.x · Cited by 97 · see citing works
Chan, J., Crowell, E. F., Eder, M., Calder, G. M., Bunnewell, S., Findlay, K., Vernhettes, S., Höfte, H., & Lloyd, C. W. (2010) · Journal of Cell Science · doi:10.1242/jcs.074641 · Cited by 95 · see citing works
Khan, M., Xu, M., Murmu, J., Tabb, P., Liu, Y., Storey, K. M., McKim, S. M., Douglas, C. J., & Hepworth, S. R. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.188573 · Cited by 93 · 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
Cho, E., & Zambryski, P. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018542108 · Cited by 91 · see citing works
Rast, M. I., & Simon, R. (2012) · The Plant Cell · doi:10.1105/tpc.112.099978 · Cited by 89 · see citing works
Self-citationRBE controls microRNA164 expression to effect floral organogenesis
Huang, T., López‐Giráldez, F., Townsend, J. P., & Irish, V. F. (2012) · Development · doi:10.1242/dev.075069 · Cited by 86 · see citing works
Organ abscission: exit strategies require signals and moving traffic
Liljegren, S. J. (2012) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2012.09.012 · Cited by 84 · see citing works
PETAL LOSS is a boundary gene that inhibits growth between developing sepals in Arabidopsis thaliana
Lampugnani, E. R., Kilinc, A., & Smyth, D. R. (2012) · The Plant Journal · doi:10.1111/j.1365-313x.2012.05023.x · Cited by 81 · see citing works
Besnard, F., Vernoux, T., & Hamant, O. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0732-4 · Cited by 62 · see citing works
Nibau, C., Stilio, V. S. D., Wu, H., & Cheung, A. Y. (2010) · Journal of Experimental Botany · doi:10.1093/jxb/erq325 · Cited by 62 · see citing works
Khan, M., Tabb, P., & Hepworth, S. R. (2012) · Plant Signaling & Behavior · doi:10.4161/psb.20599 · Cited by 61 · see citing works
Ha, C. M., Jun, J. H., & Fletcher, J. C. (2010) · Genetics · doi:10.1534/genetics.110.118703 · Cited by 60 · see citing works
Bureau, M., Rast, M. I., Illmer, J., & Simon, R. (2010) · Plant Molecular Biology · doi:10.1007/s11103-010-9688-2 · Cited by 56 · see citing works
Self-citationLandrein, B., Lathe, R. S., Bringmann, M., Vouillot, C., Ivakov, A. A., Boudaoud, A., Persson, S., & Hamant, O. (2013) · Current Biology · doi:10.1016/j.cub.2013.04.013 · Cited by 55 · see citing works
Lei, L., Li, S., & Gu, Y. (2012) · Plant Signaling & Behavior · doi:10.4161/psb.20338 · Cited by 52 · see citing works
Sun, X., Feng, Z., Meng, L., Zhu, J., & Geitmann, A. (2013) · Planta · doi:10.1007/s00425-013-1844-x · Cited by 49 · see citing works
Engelhorn, J., Reimer, J. J., Leuz, I., Göbel, U., Hüettel, B., Farrona, S., & Turck, F. (2012) · Development · doi:10.1242/dev.078618 · Cited by 37 · see citing works
Butenko, M. A., Shi, C., & Aalen, R. B. (2012) · Plant Signaling & Behavior · doi:10.4161/psb.7.1.18379 · Cited by 32 · see citing works
Kim, J., & Lee, H. W. (2013) · Plant Signaling & Behavior · doi:10.4161/psb.22979 · Cited by 32 · see citing works
The ATP-Binding Cassette Transporter ABCB19 Regulates Postembryonic Organ Separation in Arabidopsis
Zhao, H., Liu, L., Mo, H., Qian, L., Cao, Y., Cui, S., Li, X., & Ma, L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060809 · Cited by 26 · see citing works
Plant Development: Brassinosteroids Go Out of Bounds
Arnaud, N., & Laufs, P. (2013) · Current Biology · doi:10.1016/j.cub.2013.01.001 · Cited by 16 · see citing works
Boundary genes in regulation and evolution of secondary growth
Yordanov, Y. S., & Busov, V. B. (2011) · Plant Signaling & Behavior · doi:10.4161/psb.6.5.14973 · Cited by 10 · see citing works
Growing Cells Push Back under Pressure
Gibson, W. T., & Gibson, M. C. (2012) · Cell · doi:10.1016/j.cell.2012.03.019 · Cited by 7 · see citing works
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Paksa, A., Bandemer, J., Höckendorf, B., Razin, N., Tarbashevich, K., Minina, S., Meyen, D., Biundo, A., Leidel, S. A., Peyriéras, N., et al. (2016) · Nature Communications · doi:10.1038/ncomms11288 · Cited by 45 · see citing works
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Quon, T., Lampugnani, E. R., & Smyth, D. R. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00152 · Cited by 29 · see citing works
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Fambrini, M., Mariotti, L., Parlanti, S., Salvini, M., & Pugliesi, C. (2015) · Plant Biology · doi:10.1111/plb.12358 · Cited by 28 · see citing works
Organ boundary NAC‐domain transcription factors are implicated in the evolution of petal fusion
Zhong, J., Powell, S., & Preston, J. C. (2016) · Plant Biology · doi:10.1111/plb.12493 · Cited by 28 · see citing works
Izhaki, A., Alvarez, J. P., Cinnamon, Y., Genin, O., Liberman-Aloni, R., & Eyal, Y. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.01126 · Cited by 27 · see citing works
VvLBD39, a grape LBD transcription factor, regulates plant response to salt and drought stress
Chen, L., Ji, X., Luo, C., Song, X., Leng, X., Ma, Y., Wang, J., Fang, J., & Ren, Y. (2024) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2024.105918 · Cited by 26 · see citing works
GDP-L-fucose is required for boundary definition in plants
Gonçalves, B., Maugarny-Calès, A., Adroher, B., Cortizo, M., Borrega, N., Blein, T., Hasson, A., Gineau, E., Mouille, G., Laufs, P., et al. (2017) · Journal of Experimental Botany · doi:10.1093/jxb/erx402 · Cited by 26 · see citing works
Jiao, K., Li, X., Guo, Y., Guan, Y., Guo, W., Luo, D., Hu, Z., & Shen, Z. (2018) · Planta · doi:10.1007/s00425-018-3038-z · Cited by 24 · see citing works
He, L., Liu, Y., Mao, Y., Wu, X., Zheng, X., Zhao, W., Mo, X., Wang, R., Wu, Q., Wang, D., et al. (2024) · The Plant Cell · doi:10.1093/plcell/koae033 · Cited by 22 · see citing works
Frond architecture of the rootless duckweed Wolffia globosa
Yang, J., Zhao, X., Li, G., Hu, S., & Hou, H. (2021) · BMC Plant Biology · doi:10.1186/s12870-021-03165-5 · Cited by 21 · see citing works
The founder-cell transcriptome in the Arabidopsis apetala1 cauliflower inflorescence meristem
Frerichs, A., Thoma, R., Abdallah, A. T., Frommolt, P., Werr, W., & Chandler, J. (2016) · BMC Genomics · doi:10.1186/s12864-016-3189-x · Cited by 21 · see citing works
A systems approach to understand shoot branching
Tian, C., & Jiao, Y. (2015) · Current Plant Biology · doi:10.1016/j.cpb.2015.08.001 · Cited by 20 · see citing works
KNOX Genes Were Involved in Regulating Axillary Bud Formation of Chrysanthemum × morifolium
Yang, Q., Cong, T., Yao, Y., Cheng, T., Yuan, C., & Zhang, Q. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087081 · Cited by 19 · see citing works
Butenko, M. A., & Simon, R. G. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv310 · Cited by 19 · see citing works
Self-citationMolecular Mechanisms of Floral Boundary Formation in Arabidopsis
Yu, H., & Huang, T. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17030317 · Cited by 18 · see citing works
The vascular plants: open system of growth
Basile, A., Fambrini, M., & Pugliesi, C. (2017) · Development Genes and Evolution · doi:10.1007/s00427-016-0572-1 · Cited by 17 · see citing works
The Ha‐ROXL gene is required for initiation of axillary and floral meristems in sunflower
Basile, A., Fambrini, M., Tani, C., Shukla, V., Licausi, F., & Pugliesi, C. (2019) · genesis · doi:10.1002/dvg.23307 · Cited by 16 · see citing works
Matos, J. L., & Bergmann, D. C. (2014) · F1000Prime Reports · doi:10.12703/p6-53 · Cited by 15 · see citing works
Molecular Regulation of Shoot Architecture in Soybean
Hou, Z., Huang, H. C., Wang, Y., Chen, L., Yue, L., Liu, B., Kong, F., & Hui, Y. (2024) · Plant Cell & Environment · doi:10.1111/pce.15138 · Cited by 14 · see citing works
Roles of BdUNICULME4 and BdLAXATUM‐A in the non‐domesticated grass Brachypodium distachyon
Magne, K., Liu, S., Massot, S., Dalmais, M., Morin, H., Sibout, R., Bendahmane, A., & Ratet, P. (2020) · The Plant Journal · doi:10.1111/tpj.14758 · Cited by 14 · see citing works
Fujihara, R., Uchida, N., Tameshige, T., Kawamoto, N., Hotokezaka, Y., Higaki, T., Simon, R. G., Torii, K. U., Tasaka, M., & Aida, M. (2021) · Plant Biotechnology · doi:10.5511/plantbiotechnology.21.0508a · Cited by 14 · see citing works
Self-citationColling, J., Tohge, T., Clercq, R. D., Brunoud, G., Vernoux, T., Fernie, A. R., Makunga, N. P., Goossens, A., & Pauwels, L. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv291 · Cited by 13 · see citing works
Xu, L., Fang, N., Lu, T., Tameshige, T., Nakata, M. T., Jiang, Y., Tan, L., He, H. Y., Zhang, X., Huang, Y., et al. (2024) · Journal of Experimental Botany · doi:10.1093/jxb/erae443 · Cited by 12 · see citing works
Shen, D., Kulikova, O., Gühl, K., Franssen, H., Kohlen, W., Bisseling, T., & Geurts, R. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-2194-z · Cited by 12 · see citing works
The Secrets of Meristems Initiation: Axillary Meristem Initiation and Floral Meristem Initiation
Yang, Q., Yuan, C., Cong, T., & Zhang, Q. (2023) · Plants · doi:10.3390/plants12091879 · Cited by 11 · see citing works
LEAFDATA: a literature-curated database for Arabidopsis leaf development
Szakonyi, D. (2016) · Plant Methods · doi:10.1186/s13007-016-0115-9 · Cited by 11 · see citing works
Brachypodium distachyon UNICULME4 and LAXATUM-A are redundantly required for development
Liu, S., Magne, K., Daniel, S., Sibout, R., & Ratet, P. (2021) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiab456 · Cited by 11 · see citing works
Fambrini, M., Salvini, M., & Pugliesi, C. (2016) · Development Genes and Evolution · doi:10.1007/s00427-016-0571-2 · Cited by 11 · see citing works
Nodule diversity, evolution, organogenesis and identity
Liu, S., Ratet, P., & Magne, K. (2020) · Advances in botanical research · doi:10.1016/bs.abr.2019.09.009 · Cited by 10 · see citing works
Building beauty: Understanding how hormone signaling regulates petal patterning and morphogenesis
Salvi, E., & Moyroud, E. (2025) · The Plant Journal · doi:10.1111/tpj.70101 · Cited by 9 · see citing works
Non-cell-autonomous signaling associated with barley ALOG1 specifies spikelet meristem determinacy
Jiang, G., Koppolu, R., Rutten, T. L. M., Hensel, G., Lundqvist, U., Moya, Y. A. T., Huang, Y., Rajaraman, J., Poursarebani, N., Nicolaus Von Wirén, A., et al. (2024) · Current Biology · doi:10.1016/j.cub.2024.04.083 · Cited by 9 · see citing works
The Genetic Control of the Compound Leaf Patterning in Medicago truncatula
Mo, X., He, L., Liu, Y., Wang, D., Zhao, B., & Chen, J. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2021.749989 · Cited by 10 · see citing works
Single-cell transcriptome sequencing reveals the mechanism regulating rice plumule development
Zhu, M., Zhang, M., Huang, K., Lu, F., Wang, H., Zhao, S., Yu, Y., Tang, S., Wu, H., Hu, P., et al. (2024) · The Crop Journal · doi:10.1016/j.cj.2024.04.009 · Cited by 8 · see citing works
Garrido, A. N., Supijono, E., Boshara, P., Douglas, S. J., Stronghill, P. E., Li, B., Nambara, E., Kliebenstein, D. J., & Riggs, C. D. (2020) · The Plant Journal · doi:10.1111/tpj.14878 · Cited by 8 · see citing works
Chen, X., Lei, T., Yan, Y., Sun, M., Zhong, T., Wu, B., Liu, H., Zhang, C., Sun, F., & Xi, Y. (2024) · Plants · doi:10.3390/plants13223237 · Cited by 7 · see citing works
Characterization of Top Leader Elongation in Nordmann Fir (Abies nordmanniana)
Martens, H. J., Sørensen, S., Burow, M., & Veierskov, B. (2019) · Journal of Plant Growth Regulation · doi:10.1007/s00344-019-09938-5 · Cited by 7 · see citing works
Kohler, A., Scheil, A., Hill, J. L., Allen, J. R., Al-Haddad, J. M., Goeckeritz, C. Z., Strader, L. C., Telewski, F. W., & Hollender, C. A. (2024) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiae085 · Cited by 7 · see citing works
Genome-wide identification and evolutionary view of ALOG gene family in Solanaceae
Turchetto, C., Silvério, A. D. C., Waschburger, E. L., Lacerda, M. E. G., Quintana, I. V., & Turchetto‐Zolet, A. C. (2023) · Genetics and Molecular Biology · doi:10.1590/1415-4757-gmb-2023-0142 · Cited by 6 · see citing works
Pautot, V., Berbel, A., Cayla, T., Eschstruth, A., Adroher, B., Ratet, P., Madueño, F., & Laufs, P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232214114 · Cited by 6 · see citing works
Caselli, F., Ferrario, C., Beretta, V. M., Tondepu, S. A. G., Dumas, R., Herrera‐Ubaldo, H., de Folter, S., Kater, M. M., & Gregis, V. (2025) · The Plant Journal · doi:10.1111/tpj.70041 · Cited by 5 · see citing works
Diversity of flowers in basic structure and its underlying molecular mechanisms
Wang, H., ZHANG, R., Cheng, J., Duan, X., Zhao, H., HongYan, S. H. A. N., & Kong, H. (2019) · Scientia Sinica Vitae · doi:10.1360/n052018-00219 · Cited by 4 · see citing works
Shen, D., Holmer, R., Kulikova, O., Mannapperuma, C., Street, N. R., Yan, Z., van der Maden, T., Bu, F., Zhang, Y., Geurts, R., et al. (2021) · The Plant Journal · doi:10.1111/tpj.15242 · Cited by 5 · see citing works
Ercoli, M. F., Shigenaga, A. M., de Araújo, A. T., Jain, R., & Ronald, P. C. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.02.02.578681 · Cited by 5 · see citing works
Insight into the formation of trumpet and needle-type leaf in Ginkgo biloba L. mutant
Tang, F., Sun, P., Zhang, Q., Zhong, F., Wang, Y., & Lu, M. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.1081280 · Cited by 4 · see citing works
Ovule number as a rising star for regulating seed yield: Hope or hype
Khan, S. U., Ali, A. R., Saeed, S., Fan, Y., Shehazd, A., Gul, H., Fahad, S., & Lu, K. (2024) · Journal of Integrative Agriculture · doi:10.1016/j.jia.2024.02.013 · Cited by 4 · see citing works
CUC genes control boundary domains for shoot meristem maintenance and organ initiation in maize
Zhong, W., Dong, L., Zhang, G., Li, Z., Wang, Q., Jackson, D. P., & Yang, F. (2025) · New Phytologist · doi:10.1111/nph.70441 · Cited by 3 · see citing works
Li, J., Wen, X., Zhang, Q., Tian, Y., Pu, Y., Wang, J., Liu, B., Du, Y., & Dai, S. (2024) · Horticulture Research · doi:10.1093/hr/uhae039 · Cited by 3 · see citing works
Wang, X., Liu, H., Wei, H., Wang, K., ZHANG, N., & Si, H. (2026) · Plant Science · doi:10.1016/j.plantsci.2026.113006 · Cited by 2 · see citing works
Oud, S., Zurowski, M. M., van der Jagt, P. L., Yeo, M. T. S., Walker, J. F., Moyroud, E., & Vroomans, R. M. A. (2026) · Development · doi:10.1242/dev.205745 · Cited by 3 · see citing works
Ercoli, M. F., Shigenaga, A. M., de Araújo, A. T., Louie, K., Bowen, B. P., Weitz, T. S., Ramesh, S., Jain, R., Northen, T. R., & Ronald, P. C. (2026) · The Plant Cell · doi:10.1093/plcell/koag180 · Cited by 7 · see citing works
Brassinosteroids' regulation of plant architecture
Song, X., Qi, Z., Ahammed, G. J., Yu, J., & Xia, X. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-813227-2.00016-3 · Cited by 2 · see citing works
Genetics and development of pseudanthia in the genus Helianthus: A review
Rogo, U., Fambrini, M., Pugliesi, C., & Simoni, S. (2025) · Biologia · doi:10.1007/s11756-025-02024-0 · Cited by 1 · see citing works
- Authors
- Žádníková, P., & Simon, R.
- Affiliations
- Cluster of Excellence on Plant Sciences (DE)
- Corresponding author
- Simon, Rüdiger
- Venue
- Current Opinion in Plant Biology
- Publisher
- Elsevier BV
- Published
- 2014-02
- Volume
- 17
- Pages
- 116-125
- ISSN
- 1369-5266 (ISSN-L)
- OpenAlex
- W2082421148
- Cited by
- 121
- References
- 51
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 11 · 2023: 7 · 2022: 8 · 2021: 12 · 2020: 12 · 2019: 6 · 2018: 9 · 2017: 11 · 2016: 11 · 2015: 13 · 2014: 8
- FWCI
- 1.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Current Opinion in Plant Biology (publishedVersion)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- shoot apical meristem, organogenesis, stem cell proliferation, cell-to-cell signaling, gene regulatory networks, transcription factors, hormone crosstalk, physical stress, plant organ development
- MeSH terms
- Models, Biological, Plant Proteins, Stem Cells, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Meristem, Plant Shoots, Cell Proliferation, Gene Regulatory Networks, Plant Development
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