MOLECULAR AND CELLULAR MECHANISMS OF STEM CELL MAINTENANCE IN PLANT MERISTEMS: A LITERATURE REVIEW

Authors

  • Awanda Prasono Universitas Riau

DOI:

https://doi.org/10.31849/bl.v12i1.26721

Keywords:

Plant Stem Cells, Meristem Cell Fate, Transcriptional Regulation, Epigenetics

Abstract

Plant meristems harbor stem cells that maintain their capacity for self-renewal while generating daughter cells that differentiate into various tissues and organs. This delicate balance between self-renewal and differentiation is governed by complex molecular and cellular mechanisms. This literature review synthesizes recent advances in understanding the regulatory networks controlling stem cell maintenance in plant meristems, focusing on the shoot apical meristem (SAM), root apical meristem (RAM), and cambium. The review examines key signaling pathways, transcriptional networks, epigenetic regulation, hormonal control, and cellular communication mechanisms that coordinate stem cell maintenance. Recent technological advances in single-cell sequencing, live imaging, and computational modeling have revealed unprecedented insights into meristem function. Understanding these mechanisms has important implications for crop improvement, sustainable agriculture, and plant adaptation to changing environments. This comprehensive review integrates findings from over 50 recent studies to provide a current understanding of the molecular and cellular basis of plant stem cell maintenance

References

Achard, P., Gusti, A., Cheminant, S., Alioua, M., Dhondt, S., Coppens, F., Beemster, G. T., & Genschik, P. (2009). Gibberellin signaling controls cell proliferation rate in Arabidopsis. Current Biology, 19(14), 1188-1193. https://doi.org/10.1016/j.cub.2009.05.059
Aichinger, E., Kornet, N., Friedrich, T., & Laux, T. (2012). Plant stem cell niches. Annual Review of Plant Biology, 63, 615-636. https://doi.org/10.1146/annurev-arplant-042811-105555
Ariel, F., Lucero, L., Christ, A., Mammarella, M. F., Jegu, T., Veluchamy, A., Mariappan, K., Latrasse, D., Blein, T., Liu, C., Benhamed, M., & Crespi, M. (2020). R-loop mediated trans action of the APOLO long noncoding RNA. Molecular Cell, 77(5), 1055-1065. https://doi.org/10.1016/j.molcel.2019.12.015
Bolduc, N., Yilmaz, A., Mejia-Guerra, M. K., Morohashi, K., O'Connor, D., Grotewold, E., & Hake, S. (2012). Unraveling the KNOTTED1 regulatory network in maize meristems. Genes & Development, 26(15), 1685-1690. https://doi.org/10.1101/gad.193433.112
Bowman, J. L., Kohchi, T., Yamato, K. T., Jenkins, J., Shu, S., Ishizaki, K., Yamaoka, S., Nishihama, R., Nakamura, Y., Berger, F., Adam, C., Aki, S. S., Althoff, F., Araki, T., Arteaga-Vazquez, M. A., Balasubrmanian, S., Barry, K., Bauer, D., Boehm, C. R., ... Schmutz, J. (2017). Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell, 171(2), 287-304. https://doi.org/10.1016/j.cell.2017.09.030
Brackmann, K., Qi, J., Gebert, M., Jouannet, V., Schlamp, T., Grünwald, K., Wallner, E. S., Novikova, D. D., Levitsky, V. G., Agustí, J., Sanchez, P., Lohmann, J. U., & Greb, T. (2018). Spatial specificity of auxin responses coordinates wood formation. Nature Communications, 9(1), 875. https://doi.org/10.1038/s41467-018-03256-2
Burian, A., Barbier de Reuille, P., & Kuhlemeier, C. (2016). Patterns of stem cell divisions contribute to plant longevity. Current Biology, 26(11), 1385-1394. https://doi.org/10.1016/j.cub.2016.03.067
Bustamante, M., Matus, J. T., & Riechmann, J. L. (2016). Genome-wide analyses for dissecting gene regulatory networks in the shoot apical meristem. Journal of Experimental Botany, 67(6), 1639-1648. https://doi.org/10.1093/jxb/erw058
Cao, L., Shi, Y., & Zhu, W. (2020). Regulatory mechanisms of the stem cell niche during plant organ development. Journal of Integrative Plant Biology, 62(7), 884-896. https://doi.org/10.1111/jipb.12950
Casal, J. J. (2013). Photoreceptor signaling networks in plant responses to shade. Annual Review of Plant Biology, 64, 403-427. https://doi.org/10.1146/annurev-arplant-050312-120221
Chaiwanon, J., Wang, W., Zhu, J. Y., Oh, E., & Wang, Z. Y. (2016). Information integration and communication in plant growth regulation. Cell, 164(6), 1257-1268. https://doi.org/10.1016/j.cell.2016.01.044
Chickarmane, V. S., Gordon, S. P., Tarr, P. T., Heisler, M. G., & Meyerowitz, E. M. (2012). Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proceedings of the National Academy of Sciences, 109(10), 4002-4007. https://doi.org/10.1073/pnas.1200636109
Choudhary, A., Kumar, A., & Kaur, N. (2020). ROS and oxidative burst: Roots in plant development. Plant Diversity, 42(1), 33-43. https://doi.org/10.1016/j.pld.2019.10.002
Daum, G., Medzihradszky, A., Suzaki, T., & Lohmann, J. U. (2014). A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis. Proceedings of the National Academy of Sciences, 111(40), 14619-14624. https://doi.org/10.1073/pnas.1406446111
de Lucas, M., Pu, L., Turco, G., Gaudinier, A., Morao, A. K., Harashima, H., Kim, D., Ron, M., Sugimoto, K., Roudier, F., & Brady, S. M. (2016). Transcriptional regulation of Arabidopsis polycomb repressive complex 2 coordinates cell-type proliferation and differentiation. The Plant Cell, 28(10), 2616-2631. https://doi.org/10.1105/tpc.15.00744
Dello Ioio, R., Nakamura, K., Moubayidin, L., Perilli, S., Taniguchi, M., Morita, M. T., Aoyama, T., Costantino, P., & Sabatini, S. (2008). A genetic framework for the control of cell division and differentiation in the root meristem. Science, 322(5906), 1380-1384. https://doi.org/10.1126/science.1164147
Di Mambro, R., De Ruvo, M., Pacifici, E., Salvi, E., Sozzani, R., Benfey, P. N., Busch, W., Novak, O., Ljung, K., Di Paola, L., Marée, A. F. M., Costantino, P., Grieneisen, V. A., & Sabatini, S. (2017). Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. Proceedings of the National Academy of Sciences, 114(36), E7641-E7649. https://doi.org/10.1073/pnas.1705833114
Di Mambro, R., Svolacchia, N., Dello Ioio, R., Pierdonati, E., Salvi, E., Pedrazzini, E., Vitale, A., Perilli, S., Sozzani, R., Benfey, P. N., Busch, W., Novak, O., Ljung, K., Di Paola, L., Marée, A. F. M., Costantino, P., Grieneisen, V. A., & Sabatini, S. (2019). The molecular basis of cytokinin function. Science, 366(6464), 443-448. https://doi.org/10.1126/science.aaw5197
Drisch, R. C., & Stahl, Y. (2015). Function and regulation of transcription factors involved in root apical meristem and stem cell maintenance. Frontiers in Plant Science, 6, 505. https://doi.org/10.3389/fpls.2015.00505
Efroni, I. (2018). A conceptual framework for cell identity transitions in plants. Plant and Cell Physiology, 59(4), 696-706. https://doi.org/10.1093/pcp/pcx172
Efroni, I., Han, S. K., Kim, H. J., Wu, M. F., Steiner, E., Birnbaum, K. D., Hong, J. C., Eshed, Y., & Wagner, D. (2013). Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Developmental Cell, 24(4), 438-445. https://doi.org/10.1016/j.devcel.2013.01.019
Efroni, I., Mello, A., Nawy, T., Ip, P. L., Rahni, R., DelRose, N., Powers, A., Satija, R., & Birnbaum, K. D. (2016). Root regeneration triggers an embryo-like sequence guided by hormonal interactions. Cell, 165(7), 1721-1733. https://doi.org/10.1016/j.cell.2016.04.046
Fletcher, J. C. (2018). The CLV-WUS stem cell signaling pathway: a roadmap to crop yield optimization. Plants, 7(4), 87. https://doi.org/10.3390/plants7040087
Frank, M. H., & Scanlon, M. J. (2015). Transcriptomic evidence for the evolution of shoot meristem function in sporophyte-dominant land plants through concerted selection of ancestral gametophytic and sporophytic genetic programs. Molecular Biology and Evolution, 32(2), 355-367. https://doi.org/10.1093/molbev/msu303
Gaillochet, C., & Lohmann, J. U. (2015). The never-ending story: from pluripotency to plant developmental plasticity. Development, 142(13), 2237-2249. https://doi.org/10.1242/dev.117614
Gaillochet, C., Daum, G., & Lohmann, J. U. (2015). O cell, where art thou? The mechanisms of shoot meristem patterning. Current Opinion in Plant Biology, 23, 91-97. https://doi.org/10.1016/j.pbi.2014.11.002
Greb, T., & Lohmann, J. U. (2016). Plant stem cells. Current Biology, 26(17), R816-R821. https://doi.org/10.1016/j.cub.2016.07.070
Guan, C., Wu, B., Yu, T., Wang, Q., Krogan, N. T., Liu, X., & Jiao, Y. (2017). Spatial auxin signaling controls leaf flattening in Arabidopsis. Current Biology, 27(19), 2940-2950. https://doi.org/10.1016/j.cub.2017.08.042
Guo, Y., Han, L., Hymes, M., Denver, R., & Clark, S. E. (2010). CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. The Plant Journal, 63(6), 889-900. https://doi.org/10.1111/j.1365-313X.2010.04295.x
Han, X., Huang, X., & Hughes, J. (2018). Signalling and functional diversity within the Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE family. Journal of Integrative Plant Biology, 60(8), 672-687. https://doi.org/10.1111/jipb.12652
Heidstra, R., & Sabatini, S. (2014). Plant and animal stem cells: similar yet different. Nature Reviews Molecular Cell Biology, 15(5), 301-312. https://doi.org/10.1038/nrm3790
Jürgens, G. (2018). Shoot and root meristem maintenance in Arabidopsis. Plant Sciences, 18, 53-76. https://doi.org/10.1007/978-3-319-93733-0_4
Kajala, K., Ramakrishna, P., Fisher, A., Bergmann, D. C., De Smet, I., Sozzani, R., Weijers, D., & Brady, S. M. (2014). Omics and modelling approaches for understanding regulation of asymmetric cell divisions in Arabidopsis and other angiosperm plants. Annals of Botany, 113(7), 1083-1105. https://doi.org/10.1093/aob/mcu065
Kitagawa, M., & Jackson, D. (2017). Plasmodesmata-mediated cell-to-cell communication in the shoot apical meristem: how stem cells talk. Plants, 6(1), 12. https://doi.org/10.3390/plants6010012
Knauer, S., Holt, A. L., Rubio-Somoza, I., Tucker, E. J., Hinze, A., Pisch, M., Javelle, M., Timmermans, M. C., Tucker, M. R., & Laux, T. (2013). A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Developmental Cell, 24(2), 125-132. https://doi.org/10.1016/j.devcel.2012.12.009
Kong, X., Tian, H., Yu, Q., Zhang, F., Wang, R., Gao, S., Xu, W., Liu, J., Shani, E., Fu, C., Zhou, J., Gou, X., Li, G., Ding, Z. (2018). PHB3 maintains root stem cell niche identity through ROS-responsive AP2/ERF transcription factors in Arabidopsis. Cell Reports, 22(5), 1350-1363. https://doi.org/10.1016/j.celrep.2017.12.105
Landrein, B., & Hamant, O. (2013). How mechanical stress controls meristem size. Current Opinion in Plant Biology, 16(6), 730-737. https://doi.org/10.1016/j.pbi.2013.07.005
Landrein, B., Kiss, A., Sassi, M., Chauvet, A., Das, P., Cortizo, M., Laufs, P., Takeda, S., Aida, M., Traas, J., Vernoux, T., Boudaoud, A., & Hamant, O. (2015). Mechanical stress contributes to the expression of the STM homeobox gene in Arabidopsis shoot meristems. eLife, 4, e07811. https://doi.org/10.7554/eLife.07811
Lastdrager, J., Hanson, J., & Smeekens, S. (2014). Sugar signals and the control of plant growth and development. Journal of Experimental Botany, 65(3), 799-807. https://doi.org/10.1093/jxb/ert474
Li, L., Verstraeten, I., Ferniez, A. P., Vissenberg, K., & Geelen, D. (2019). Cell wall modifications of root cells under salinity and drought stress. Colloids and Surfaces B: Biointerfaces, 177, 23-29. https://doi.org/10.1016/j.colsurfb.2019.01.055
Long, Y., Goedhart, J., Schneijderberg, M., Terpstra, I., Shimotohno, A., Bouchet, B. P., Heidstra, R., Scheres, B., & Blilou, I. (2015). SCARECROW-LIKE23 and SCARECROW jointly specify endodermal cell fate but distinctly control SHORT-ROOT movement. The Plant Journal, 84(4), 773-784. https://doi.org/10.1111/tpj.13038
Ma, Y., Miotk, A., Šutiković, Z., Ermakova, O., Wenzl, C., Medzihradszky, A., Gaillochet, C., Forner, J., Utan, G., Brackmann, K., Galvan-Ampudia, C. S., Vernoux, T., Greb, T., & Lohmann, J. U. (2019). WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis. Nature Communications, 10(1), 5093. https://doi.org/10.1038/s41467-019-13074-9
Mayer, K. F., Waugh, R., Brown, J. W., Schulman, A., Langridge, P., Platzer, M., Fincher, G. B., Muehlbauer, G. J., Sato, K., Close, T. J., Wise, R. P., & Stein, N. (2013). A physical, genetic and functional sequence assembly of the barley genome. Nature, 491(7426), 711-716. https://doi.org/10.1038/nature11543
Miyashima, S., Roszak, P., Sevilem, I., Toyokura, K., Blob, B., Heo, J. O., Mellor, N., Help-Rinta-Rahko, H., Otero, S., Smet, W., Boekschoten, M., Hooiveld, G., Hashimoto, K., Smetana, O., Siligato, R., Wallner, E. S., Mähönen, A. P., Kondo, Y., Melnyk, C. W., ... Helariutta, Y. (2019). Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature, 565(7740), 490-494. https://doi.org/10.1038/s41586-018-0839-y
Moreno-Risueno, M. A., Sozzani, R., Yardımcı, G. G., Petricka, J. J., Vernoux, T., Blilou, I., Alonso, J., Winter, C. M., Ohler, U., Scheres, B., & Benfey, P. N. (2015). Transcriptional control of tissue formation throughout root development. Science, 350(6259), 426-430. https://doi.org/10.1126/science.aad1171
Murphy, E., Smith, S., & De Smet, I. (2012). Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. The Plant Cell, 24(8), 3198-3217. https://doi.org/10.1105/tpc.112.099010
Nieminen, K., Blomster, T., Helariutta, Y., & Mähönen, A. P. (2015). Vascular cambium development. The Arabidopsis Book, 13, e0177. https://doi.org/10.1199/tab.0177
Nimchuk, Z. L. (2017). CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two-step transcriptional compensation loop. PLOS Genetics, 13(3), e1006681. https://doi.org/10.1371/journal.pgen.1006681
Nuccio, M. L., Wu, J., Mowers, R., Zhou, H. P., Meghji, M., Primavesi, L. F., Paul, M. J., Chen, X., Gao, Y., Haque, E., Basu, S. S., & Lagrimini, L. M. (2015). Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nature Biotechnology, 33(8), 862-869. https://doi.org/10.1038/nbt.3277
Perales, M., & Reddy, G. V. (2012). Stem cell maintenance in shoot apical meristems. Current Opinion in Plant Biology, 15(1), 10-16. https://doi.org/10.1016/j.pbi.2011.10.008
Perilli, S., Di Mambro, R., & Sabatini, S. (2012). Growth and development of the root apical meristem. Current Opinion in Plant Biology, 15(1), 17-23. https://doi.org/10.1016/j.pbi.2011.10.006
Petersson, S. V., Johansson, A. I., Kowalczyk, M., Makoveychuk, A., Wang, J. Y., Moritz, T., Grebe, M., Benfey, P. N., Sandberg, G., & Ljung, K. (2009). An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. The Plant Cell, 21(6), 1659-1668. https://doi.org/10.1105/tpc.109.066480
Pillitteri, L. J., Guo, X., & Dong, J. (2016). Asymmetric cell division in plants: mechanisms of symmetry breaking and cell fate determination. Cellular and Molecular Life Sciences, 73(22), 4213-4229. https://doi.org/10.1007/s00018-016-2290-2
Rahni, R., Efroni, I., & Birnbaum, K. D. (2016). A case for distributed control of local stem cell behavior in plants. Developmental Cell, 38(6), 635-642. https://doi.org/10.1016/j.devcel.2016.08.015
Rodriguez-Leal, D., Lemmon, Z. H., Man, J., Bartlett, M. E., & Lippman, Z. B. (2017). Engineering quantitative trait variation for crop improvement by genome editing. Cell, 171(2), 470-480. https://doi.org/10.1016/j.cell.2017.08.030
Sablowski, R. (2007). The dynamic plant stem cell niches. Current Opinion in Plant Biology, 10(6), 639-644. https://doi.org/10.1016/j.pbi.2007.07.001
Sablowski, R. (2011). Plant stem cell niches: from signalling to execution. Current Opinion in Plant Biology, 14(1), 4-9. https://doi.org/10.1016/j.pbi.2010.08.001
Santuari, L., Sanchez-Perez, G. F., Luijten, M., Rutjens, B., Terpstra, I., Berke, L., Gorte, M., Prasad, K., Bao, D., Timmermans-Hereijgers, J. L. P. M., Maeo, K., Nakamura, K., Shimotohno, A., Pencik, A., Novak, O., Ljung, K., van Heesch, S., de Bruijn, E., Cuppen, E., ... Heidstra, R. (2016). The PLETHORA gene regulatory network guides growth and cell differentiation in Arabidopsis roots. The Plant Cell, 28(12), 2937-2951. https://doi.org/10.1105/tpc.16.00656
Schaller, G. E., Street, I. H., & Kieber, J. J. (2015). Cytokinin and the cell cycle. Current Opinion in Plant Biology, 21, 7-15. https://doi.org/10.1016/j.pbi.2014.05.015
Serrano-Mislata, A., Schiessl, K., & Sablowski, R. (2021). Active control of cell size generates spatial detail during plant organogenesis. Current Biology, 31(4), 1-13. https://doi.org/10.1016/j.cub.2020.12.054
Shor, E., Paik, I., Kangisser, S., Green, R., & Huq, E. (2017). PHYTOCHROME INTERACTING FACTORS mediate metabolic control of the circadian system in Arabidopsis. New Phytologist, 215(1), 217-228. https://doi.org/10.1111/nph.14579
Smet, W., Sevilem, I., de Luis Balaguer, M. A., Wybouw, B., Mor, E., Miyashima, S., Blob, B., Roszak, P., Jacobs, T. B., Boekschoten, M., Hooiveld, G., Sozzani, R., Helariutta, Y., & De Rybel, B. (2019). DOF2.1 controls cytokinin-dependent vascular cell proliferation downstream of TMO5/LHW. Current Biology, 29(3), 520-529. https://doi.org/10.1016/j.cub.2018.12.041
Somssich, M., Je, B. I., Simon, R., & Jackson, D. (2016). CLAVATA-WUSCHEL signaling in the shoot meristem. Development, 143(18), 3238-3248. https://doi.org/10.1242/dev.133645
Su, Y. H., Liu, Y. B., & Zhang, X. S. (2011). Auxin-cytokinin interaction regulates meristem development. Molecular Plant, 4(4), 616-625. https://doi.org/10.1093/mp/ssr007
Sun, B., Looi, L. S., Guo, S., He, Z., Gan, E. S., Huang, J., Xu, Y., Wee, W. Y., & Ito, T. (2014). Timing mechanism dependent on cell division is invoked by Polycomb eviction in plant stem cells. Science, 343(6170), 1248559. https://doi.org/10.1126/science.1248559
Tucker, M. R., Roodbarkelari, F., Truernit, E., Adamski, N. M., Hinze, A., Lohmüller, B., Würschum, T., & Laux, T. (2020). Accession-specific modifiers act with ZWILLE/ARGONAUTE10 to maintain shoot meristem stem cells during embryogenesis in Arabidopsis. BMC Biology, 18(1), 61. https://doi.org/10.1186/s12915-020-00794-4
Vernoux, T., Brunoud, G., Farcot, E., Morin, V., Van den Daele, H., Legrand, J., Oliva, M., Das, P., Larrieu, A., Wells, D., Guédon, Y., Armitage, L., Picard, F., Guyomarc'h, S., Cellier, C., Parry, G., Koumproglou, R., Doonan, J. H., Estelle, M., ... Traas, J. (2011). The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Molecular Systems Biology, 7(1), 508. https://doi.org/10.1038/msb.2011.39
Wang, Q., Kohlen, W., Rossmann, S., Vernoux, T., & Theres, K. (2015). Auxin depletion from the leaf axil conditions competence for axillary meristem formation in Arabidopsis and tomato. The Plant Cell, 26(5), 2068-2079. https://doi.org/10.1105/tpc.114.123059
Wang, W., Li, G., Zhao, J., Chu, H., Lin, W., Zhang, D., Wang, Z., & Liang, W. (2018). DWARF TILLERs 1 regulates grain number through controlling tillering and plasma membrane integrity in rice. Plant Physiology, 177(3), 1142-1153. https://doi.org/10.1104/pp.18.00287
Wendrich, J. R., & Weijers, D. (2013). The Arabidopsis embryo as a miniature morphogenesis model. New Phytologist, 199(1), 14-25. https://doi.org/10.1111/nph.12267
Xiong, Y., & Sheen, J. (2014). The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiology, 164(2), 499-512. https://doi.org/10.1104/pp.113.229948
Xu, C., Liberatore, K. L., MacAlister, C. A., Huang, Z., Chu, Y. H., Jiang, K., Brooks, C., Ogawa-Ohnishi, M., Xiong, G., Pauly, M., Van Eck, J., Matsubayashi, Y., van der Knaap, E., & Lippman, Z. B. (2019). A cascade of CLAVATA

Downloads

Published

2025-05-27

Issue

Section

Article

How to Cite

MOLECULAR AND CELLULAR MECHANISMS OF STEM CELL MAINTENANCE IN PLANT MERISTEMS: A LITERATURE REVIEW. (2025). Bio-Lectura : Jurnal Pendidikan Biologi, 12(1), 110-126. https://doi.org/10.31849/bl.v12i1.26721