Plants, unlike animals, possess a unique developmental plasticity, that allows them to adapt to changing environmental conditions. A fundamental aspect of this plasticity is their ability to undergo postembryonic de novo organogenesis. This requires the presence of regulators that trigger and mediate specific spatiotemporal changes in developmental programs. The phytohormone cytokinin has been known as a principal regulator of plant development for more than six decades. In de novo shoot organogenesis and in vitro shoot regeneration, cytokinins are the prime candidates for the signal that determines shoot identity. Both processes of de novo shoot apical meristem development are accompanied by changes in gene expression, cell fate reprogramming, and the switching-on of the shoot-specific homeodomain regulator, WUSCHEL. Current understanding about the role of cytokinins in the shoot regeneration will be discussed.

Laboratory of Functional Genomics and Proteomics National Centre for Biomolecular Research Faculty of Science Masaryk University Brno Czechia

Mendel Centre for Plant Genomics and Proteomics Central European Institute of Technology Masaryk University Brno Czechia

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Allen M., Qin W., Moreau F., Moffatt B. (2002). Adenine phosphoribosyltransferase isoforms of Arabidopsis and their potential contributions to adenine and cytokinin metabolism. Physiol. Plantarum 115, 56–68. doi: 10.1034/j.1399-3054.2002.1150106.x PubMed DOI

Anantharaman V., Aravind L. (2001). The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem. Sci. 26, 579–582. doi: 10.1016/S0968-0004(01)01968-5 PubMed DOI

Atta R., Laurens L., Boucheron-Dubuisson E., Guivarc’h A., Carnero E., Giraudat-Pautot V., et al. . (2009). Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro . Plant J. 57, 626–644. doi: 10.1111/j.1365-313X.2008.03715.x PubMed DOI

Barrera-Rojas C. H., Rocha G. H. B., Polverari L., Pinheiro Brito D. A., Batista D. S., Notini M. M., et al. . (2020). miR156-targeted SPL10 controls Arabidopsis root meristem activity and root-derived de novo shoot regeneration via cytokinin responses. J. Exp. Bot. 71, 934–950. doi: 10.1093/jxb/erz475 PubMed DOI

Bartrina I., Otto E., Strnad M., Werner T., Schmülling T. (2011). Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in arabidopsis thaliana . Plant Cell 23, 69–80. doi: 10.1105/tpc.110.079079 PubMed DOI PMC

Beeckman T., Burssens S., Inze D. (2001). The peri-cell-cycle in arabidopsis. J. Exp. Bot. 52, 403–411. doi: 10.1093/jexbot/52.suppl_1.403 PubMed DOI

Berckmans B., Vassileva V., Schmid S. P. C., Maes S., Parizot B., Naramoto S., et al. . (2011). Auxin-dependent cell cycle reactivation through transcriptional regulation of arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell 23, 3671–3683. doi: 10.1105/tpc.111.088377 PubMed DOI PMC

Besnard F., Refahi Y., Morin V., Marteaux B., Brunoud G., Chambrier P., et al. . (2014). Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 505, 417–421. doi: 10.1038/nature12791 PubMed DOI

Bielach A., Podlešáková K., Marhavý P., Duclercq J., Cuesta C., Müller B., et al. . (2012). Spatiotemporal regulation of lateral root organogenesis in arabidopsis by cytokinin. Plant Cell 24, 3967–3981. doi: 10.1105/tpc.112.103044 PubMed DOI PMC

Bilyeu K. D., Cole J. L., Laskey J. G., Riekhof W. R., Esparza T. J., Kramer M. D., et al. . (2001). Molecular and biochemical characterization of a cytokinin oxidase from maize. Plant Physiol. 125, 378–386. doi: 10.1104/pp.125.1.378 PubMed DOI PMC

Bleckmann A., Weidtkamp-Peters S., Seidel C. A. M., Simon R. (2009). Stem cell signaling in arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol. 152, 166–176. doi: 10.1104/pp.109.149930 PubMed DOI PMC

Brzobohaty B., Moore I., Kristoffersen P., Bako L., Campos N., Schell J., et al. . (1993). Release of active cytokinin by a beta-glucosidase localized to the maize root-meristem. Science 262, 1051–1054. doi: 10.1126/science.8235622 PubMed DOI

Buechel S., Leibfried A., To J. P. C., Zhao Z., Andersen S. U., Kieber J. J., et al. . (2010). Role of A-type ARABIDOPSIS RESPONSE REGULATORS in meristem maintenance and regeneration. Eur. J. Cell Biol. 89, 279–284. doi: 10.1016/j.ejcb.2009.11.016 PubMed DOI

Casimiro I., Marchant A., Bhalerao R. P., Beeckman T., Dhooge S., Swarup R., et al. . (2001). Auxin transport promotes arabidopsis lateral root initiation. Plant Cell 13, 843–852. doi: 10.1105/tpc.13.4.843 PubMed DOI PMC

Chandler J. W., Werr W. (2015). Cytokinin-auxin crosstalk in cell type specification. Trends Plant Sci. 20, 291–300. doi: 10.1016/j.tplants.2015.02.003 PubMed DOI

Chatfield S. P., Capron R., Severino A., Penttila P. A., Alfred S., Nahal H., et al. . (2013). Incipient stem cell niche conversion in tissue culture: using a systems approach to probe early events in WUSCHEL-dependent conversion of lateral root primordia into shoot meristems. Plant J. 73, 798–813. doi: 10.1111/Tpj.12085 PubMed DOI

Che P., Lall S., Howell S. H. (2008). Acquiring competence for shoot development in Arabidopsis: ARR2 directly targets A-type ARR genes that are differentially activated by CIM preinCubation. Plant Signaling Behav. 3, 99–101. doi: 10.4161/psb.3.2.4958 PubMed DOI PMC

Cheng Z. J., Wang L., Sun W., Zhang Y., Zhou C., Su Y. H., et al. . (2012). Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3. Plant Physiol. 161, 240–251. doi: 10.1104/pp.112.203166 PubMed DOI PMC

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. Proc. Natl. Acad. Sci. U.S.A. 109, 4002–4007. doi: 10.1073/pnas.1200636109 PubMed DOI PMC

Christianson M. L., Warnick D. A. (1983). Competence and determination in the process of in vitro shoot organogenesis. Dev. Biol. 95, 288–293. doi: 10.1016/0012-1606(83)90029-5 PubMed DOI

Ckurshumova W., Smirnova T., Marcos D., Zayed Y., Berleth T. (2014). Irrepressible MONOPTEROS/ARF 5 promotes de novo shoot formation. New Phytol. 204, 556–566. doi: 10.1111/nph.13014 PubMed DOI

Cole M., Chandler J., Weijers D., Jacobs B., Comelli P., Werr W. (2009). DORNROSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo. Development 136, 1643–1651. doi: 10.1242/dev.032177 PubMed DOI

Cutcliffe J. W., Hellmann E., Heyl A., Rashotte A. M. (2011). CRFs form protein-protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain. J. Exp. Bot. 62, 4995–5002. doi: 10.1093/jxb/err199 PubMed DOI PMC

Dai X., Liu Z., Qiao M., Li J., Li S., Xiang F. (2017). ARR12 promotes de novo shoot regeneration in Arabidopsis thaliana via activation of WUSCHEL expression: ARR12 promotes shoot regeneration. J. Integr. Plant Biol. 59, 747–758. doi: 10.1111/jipb.12567 PubMed DOI

Dai X., Wang J., Wang L., Liu Z., Li Q., Cai Y., et al. . (2022). HY5 inhibits in vitro shoot stem cell niches initiation via directly repressing pluripotency and cytokinin pathways. Plant J. 110, 781–801. doi: 10.1111/tpj.15703 PubMed DOI

Daimon Y., Takabe K., Tasaka M. (2003). The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant Cell Physiol. 44, 113–121. doi: 10.1093/pcp/pcg038 PubMed DOI

Dao T. Q., Weksler N., Liu H. M.-H., Leiboff S., Fletcher J. C. (2022). Interactive CLV3, CLE16, and CLE17 signaling mediates stem cell homeostasis in the Arabidopsis shoot apical meristem. Development 134, 4131–4130. doi: 10.1242/dev.200787 PubMed DOI

Daum G., Medzihradszky A., Suzaki T., Lohmann J. U. (2014). A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis . Proc. Natl. Acad. Sci. U.S.A. 111, 14619–14624. doi: 10.1073/pnas.1406446111 PubMed DOI PMC

De Rybel B., Adibi M., Breda A. S., Wendrich J. R., Smit M. E., Novák O., et al. . (2014). Integration of growth and patterning during vascular tissue formation in Arabidopsis . Science 345. doi: 10.1126/science.1255215 PubMed DOI

De Rybel B., Vassileva V., Parizot B., Demeulenaere M., Grunewald W., Audenaert D., et al. . (2010). A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol. 20, 1697–1706. doi: 10.1016/j.cub.2010.09.007 PubMed DOI

Ding Z., Friml J. (2010). Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc. Natl. Acad. Sci. U.S.A. 107, 12046–12051. doi: 10.1073/pnas.1000672107 PubMed DOI PMC

Dubrovsky J. G., Doerner P. W., Colón-Carmona A., Rost T. L. (2000). Pericycle cell proliferation and lateral root initiation in arabidopsis. Plant Physiol. 124, 1648–1657. doi: 10.1104/pp.124.4.1648 PubMed DOI PMC

Dubrovsky J. G., Rost T. L., Colón-Carmona A., Doerner P. (2001). Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214, 30–36. doi: 10.1007/s004250100598 PubMed DOI

Feng Z., Zhu J., Du X., Cui X. (2012). Effects of three auxin-inducible LBD members on lateral root formation in Arabidopsis thaliana. Planta 236, 1227–1237. doi: 10.1007/s00425-012-1673-3 PubMed DOI

Fletcher J. C., Brand U., Running M. P., Simon R., Meyerowitz E. M. (1999). Signaling of cell fate decisions by CLAVATA3 in arabidopsis shoot meristems. Science 283, 1911–1914. doi: 10.1126/science.283.5409.1911 PubMed DOI

Fukaki H., Tameda S., Masuda H., Tasaka M. (2002). Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis: Role of SLR/IAA14 in lateral root formation. Plant J. 29, 153–168. doi: 10.1046/j.0960-7412.2001.01201.x PubMed DOI

Fukaki H., Taniguchi N., Tasaka M. (2006). PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J. 48, 380–389. doi: 10.1111/j.1365-313X.2006.02882.x PubMed DOI

Galinha C., Hofhuis H., Luijten M., Willemsen V., Blilou I., Heidstra R., et al. . (2007). PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449, 1053–1057. doi: 10.1038/nature06206 PubMed DOI

Galuszka P., Frébort I., Šebela M., Sauer P., Jacobsen S., Peč P. (2001). Cytokinin oxidase or dehydrogenase?: Mechanism of cytokinin degradation in cereals. Eur. J. Biochem. 268, 450–461. doi: 10.1046/j.1432-1033.2001.01910.x PubMed DOI

Gaudinova A., Dobrev P. I., Solcova B., Novak O., Strnad M., Friedecky D., et al. . (2005). The involvement of cytokinin oxidase/dehydrogenase and zeatin reductase in regulation of cytokinin levels in pea (Pisum sativum L.) leaves. J. Plant Growth Regul. 24, 188–200. doi: 10.1007/s00344-005-0043-9 DOI

Gordon S. P., Chickarmane V. S., Ohno C., Meyerowitz E. M. (2009). Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. U.S.A. 106, 16529–16534. doi: 10.1073/pnas.0908122106 PubMed DOI PMC

Gordon S. P., Heisler M. G., Reddy G. V., Ohno C., Das P., Meyerowitz E. M. (2007). Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134, 3539–3548. doi: 10.1242/dev.010298 PubMed DOI

Greb T., Lohmann J. U. (2016). Plant stem cells. Curr. Biol. 26, R816–R821. doi: 10.1016/j.cub.2016.07.070 PubMed DOI

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: CLV2 forms a CLE-binding receptor complex. Plant J. 63, 889–900. doi: 10.1111/j.1365-313X.2010.04295.x PubMed DOI PMC

Hibara K., Takada S., Tasaka M. (2003). CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formation: Role of CUC1 in adventitious SAM formation . Plant J. 36, 687–696. doi: 10.1046/j.1365-313X.2003.01911.x PubMed DOI

Higuchi M., Pischke M. S., Mahonen A. P., Miyawaki K., Hashimoto Y., Seki M., et al. . (2004). In planta functions of the Arabidopsis cytokinin receptor family. Proc. Natl. Acad. Sci. U.S.A. 101, 8821–8826. doi: 10.1073/pnas.04028871010402887101 PubMed DOI PMC

Hou B., Lim E.-K., Higgins G. S., Bowles D. J. (2004). N-glucosylation of cytokinins by glycosyltransferases of arabidopsis thaliana. J. Biol. Chem. 279, 47822–47832. doi: 10.1074/jbc.M409569200 PubMed DOI

Hu X., Xu L. (2016). Transcription factors WOX11/12 directly activate WOX5/7 to promote root primordia initiation and organogenesis. Plant Physiol. 172, 2363–2373. doi: 10.1104/pp.16.01067 PubMed DOI PMC

Huang W., Pitorre D., Poretska O., Marizzi C., Winter N., Poppenberger B., et al. . (2015). ALTERED MERISTEM PROGRAM1 suppresses ectopic stem cell niche formation in the shoot apical meristem in a largely cytokinin-independent manner. Plant Physiol. 167, 1471–1486. doi: 10.1104/pp.114.254623 PubMed DOI PMC

Hutchison C. E., Li J., Argueso C., Gonzalez M., Lee E., Lewis M. W., et al. . (2006). The arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18, 3073–3087. doi: 10.1105/tpc.106.045674 PubMed DOI PMC

Hwang I., Sheen J. (2001). Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389. doi: 10.1038/35096500 PubMed DOI

Ikeuchi M., Shibata M., Rymen B., Iwase A., Bågman A.-M., Watt L., et al. . (2018). A gene regulatory network for cellular reprogramming in plant regeneration. Plant Cell Physiol. 59, 770–782. doi: 10.1093/pcp/pcy013 PubMed DOI PMC

Imamura A., Kiba T., Tajima Y., Yamashino T., Mizuno T. (2003). In vivo and in vitro Characterization of the ARR11 Response Regulator Implicated in the His-to-Asp Phosphorelay Signal Transduction in Arabidopsis thaliana. Plant Cell Physiol. 44, 122–131. doi: 10.1093/pcp/pcg014 PubMed DOI

Inoue T., Higuchi M., Hashimoto Y., Seki M., Kobayashi M., Kato T., et al. . (2001). Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409, 1060–1063. doi: 10.1038/35059117 PubMed DOI

Ishida K., Yamashino T., Yokoyama A., Mizuno T. (2008). Three Type-B Response Regulators, ARR1, ARR10 and ARR12, Play Essential but Redundant Roles in Cytokinin Signal Transduction Throughout the Life Cycle of Arabidopsis thaliana. Plant Cell Physiol. 49, 47–57. doi: 10.1093/pcp/pcm165 PubMed DOI

Ishihara H., Sugimoto K., Tarr P. T., Temman H., Kadokura S., Inui Y., et al. . (2019). Primed histone demethylation regulates shoot regenerative competency. Nat. Commun. 10, 1786. doi: 10.1038/s41467-019-09386-5 PubMed DOI PMC

Jones R. J., Schreiber B. M. N. (1997). Role and function of cytokinin oxidase in plants. Plant Growth Regul. 23, 123–134. doi: 10.1023/A:1005913311266 DOI

Kakimoto T. (1996). CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274, 982–985. doi: 10.1126/science.274.5289.982 PubMed DOI

Kakimoto T. (2001). Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate : ATP/ADP isopentenyltransferases. Plant Cell Physiol. 42, 677–685. doi: 10.1093/pcp/pce112 PubMed DOI

Kareem A., Durgaprasad K., Sugimoto K., Du Y., Pulianmackal A. J., Trivedi Z. B., et al. . (2015). PLETHORA genes control regeneration by a two-step mechanism. Curr. Biol. 25, 1017–1030. doi: 10.1016/j.cub.2015.02.022 PubMed DOI PMC

Kareem A., Radhakrishnan D., Wang X., Bagavathiappan S., Trivedi Z. B., Sugimoto K., et al. . (2016). Protocol: a method to study the direct reprogramming of lateral root primordia to fertile shoots. Plant Methods 12, 27. doi: 10.1186/s13007-016-0127-5 PubMed DOI PMC

Kiba T., Aoki K., Sakakibara H., Mizuno T. (2004). Arabidopsis response regulator, ARR22, ectopic expression of which results in phenotypes similar to the wol cytokinin-receptor mutant. Plant Cell Physiol. 45, 1063–1077. doi: 10.1093/pcp/pch12845/8/1063 PubMed DOI

Kim J., Yang W., Forner J., Lohmann J. U., Noh B., Noh Y. (2018). Epigenetic reprogramming by histone acetyltransferase HAG1/AtGCN5 is required for pluripotency acquisition in Arabidopsis . EMBO J. 37, e98726. doi: 10.15252/embj.201798726 PubMed DOI PMC

Kurakawa T., Ueda N., Maekawa M., Kobayashi K., Kojima M., Nagato Y., et al. . (2007). Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445, 652–655. doi: 10.1038/nature05504 PubMed DOI

Kuroha T., Tokunaga H., Kojima M., Ueda N., Ishida T., Nagawa S., et al. . (2009). Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in arabidopsis . Plant Cell 21, 3152–3169. doi: 10.1105/tpc.109.068676 PubMed DOI PMC

Kusová A., Steinbachová L., Přerovská T., Drábková L. Z., Paleček J., Khan A., et al. . (2023). Completing the TRB family: newly characterized members show ancient evolutionary origins and distinct localization, yet similar interactions. Plant Mol. Biol. 112, 61–83. doi: 10.1007/s11103-023-01348-2 PubMed DOI PMC

Lall S., Nettleton D., DeCook R., Che P., Howell S. H. (2004). Quantitative trait loci associated with adventitious shoot formation in tissue culture and the program of shoot development in arabidopsis. Genetics 167, 1883–1892. doi: 10.1534/genetics.103.025213 PubMed DOI PMC

Lambolez A., Kawamura A., Takahashi T., Rymen B., Iwase A., Favero D. S., et al. . (2022). Warm temperature promotes shoot regeneration in arabidopsis thaliana . Plant Cell Physiol. 63, 618–634. doi: 10.1093/pcp/pcac017 PubMed DOI

Lardon R., Trinh H. K., Xu X., Vu L. D., Van De Cotte B., Pernisová M., et al. . (2022). Histidine kinase inhibitors impair shoot regeneration in Arabidopsis thaliana via cytokinin signaling and SAM patterning determinants. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.894208 PubMed DOI PMC

Lau S., Smet I. D., Kolb M., Meinhardt H., Jürgens G. (2011). Auxin triggers a genetic switch. Nat. Cell Biol. 13, 611–615. doi: 10.1038/ncb2212 PubMed DOI

Laux T. (2003). The stem cell concept in plants. Cell 113, 281–283. doi: 10.1016/S0092-8674(03)00312-X PubMed DOI

Laux T., Mayer K. F. X., Berger J., Jürgens G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis . Development 122, 87–96. doi: 10.1242/dev.122.1.87 PubMed DOI

Lee C., Clark S. E. (2015). A WUSCHEL-independent stem cell specification pathway is repressed by PHB, PHV and CNA in arabidopsis. PloS One 10, e0126006. doi: 10.1371/journal.pone.0126006 PubMed DOI PMC

Lee H. W., Kim N. Y., Lee D. J., Kim J. (2009). LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in arabidopsis. Plant Physiol. 151, 1377–1389. doi: 10.1104/pp.109.143685 PubMed DOI PMC

Lee K., Kim J. H., Park O.-S., Jung Y. J., Seo P. J. (2022). Ectopic expression of WOX5 promotes cytokinin signaling and de novo shoot regeneration. Plant Cell Rep. 41, 2415–2422. doi: 10.1007/s00299-022-02932-4 PubMed DOI

Lee D., Moffatt B. A. (1993). Purification and characterization of adenine phosphoribosyltransferase from Arabidopsis thaliana. Physiol. Plantarum 87, 483–492. doi: 10.1111/j.1399-3054.1993.tb02497.x DOI

Lee K., Park O.-S., Go J. Y., Yu J., Han J. H., Kim J., et al. . (2021). Arabidopsis ATXR2 represses de novo shoot organogenesis in the transition from callus to shoot formation. Cell Rep. 37, 109980. doi: 10.1016/j.celrep.2021.109980 PubMed DOI

Lee K., Park O.-S., Seo P. J. (2017). Arabidopsis ATXR2 deposits H3K36me3 at the promoters of LBD genes to facilitate cellular dedifferentiation. Sci. Signal. 10, eaan0316. doi: 10.1126/scisignal.aan0316 PubMed DOI

Lee K., Park O., Seo P. J. (2018). JMJ30-mediated demethylation of H3K9me3 drives tissue identity changes to promote callus formation in Arabidopsis. Plant J. 95, 961–975. doi: 10.1111/tpj.14002 PubMed DOI

Leibfried A., To J. P. C., Busch W., Stehling S., Kehle A., Demar M., et al. . (2005). WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172–1175. doi: 10.1038/nature04270 PubMed DOI

Li W., Liu H., Cheng Z. J., Su Y. H., Han H. N., Zhang Y., et al. . (2011). DNA methylation and histone modifications regulate de novo shoot regeneration in arabidopsis by modulating WUSCHEL expression and auxin signaling. PloS Genet. 7, e1002243. doi: 10.1371/journal.pgen.1002243 PubMed DOI PMC

Li W., Nguyen K. H., Ha C. V., Watanabe Y., Tran L.-S. P. (2019). Crosstalk between the cytokinin and MAX2 signaling pathways in growth and callus formation of Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 511, 300–306. doi: 10.1016/j.bbrc.2019.02.038 PubMed DOI

Liu Z., Dai X., Li J., Liu N., Liu X., Li S., et al. . (2020). The type-B cytokinin response regulator ARR1 inhibits shoot regeneration in an ARR12-dependent manner in arabidopsis. Plant Cell 32, 2271–2291. doi: 10.1105/tpc.19.00022 PubMed DOI PMC

Liu J., Hu X., Qin P., Prasad K., Hu Y., Xu L. (2018. b). The WOX11–LBD16 pathway promotes pluripotency acquisition in callus cells during de novo shoot regeneration in tissue culture. Plant Cell Physiol. 59, 739–748. doi: 10.1093/pcp/pcy010 PubMed DOI

Liu Z., Li J., Wang L., Li Q., Lu Q., Yu Y., et al. . (2016). Repression of callus initiation by the miRNA-directed interaction of auxin-cytokinin in Arabidopsis thaliana . Plant J. 87, 391–402. doi: 10.1111/tpj.13211 PubMed DOI

Liu J., Sheng L., Xu Y., Li J., Yang Z., Huang H., et al. . (2014). WOX11 and 12 Are Involved in the First-Step Cell Fate Transition during de Novo Root Organogenesis in Arabidopsis . Plant Cell 26, 1081–1093. doi: 10.1105/tpc.114.122887 PubMed DOI PMC

Liu H., Zhang H., Dong Y. X., Hao Y. J., Zhang X. S. (2018. a). DNA METHYLTRANSFERASE1 -mediated shoot regeneration is regulated by cytokinin-induced cell cycle in Arabidopsis . New Phytol. 217, 219–232. doi: 10.1111/nph.14814 PubMed DOI

Long J. A., Moan E. I., Medford J. I., Barton M. K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69. doi: 10.1038/379066a0 PubMed DOI

Lopes F. L., Galvan-Ampudia C., Landrein B. (2021). WUSCHEL in the shoot apical meristem: old player, new tricks. J. Exp. Bot. 72, 1527–1535. doi: 10.1093/jxb/eraa572 PubMed DOI

Mahonen A. P., Bishopp A., Higuchi M., Nieminen K. M., Kinoshita K., Tormakangas K., et al. . (2006). Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311, 94–98. doi: 10.1126/science.1118875 PubMed DOI

Malamy J. E., Benfey P. N. (1997). Organization and cell differentiation in lateral roots of Arabidopsis thaliana . Development 124, 33–44. doi: 10.1242/dev.124.1.33 PubMed DOI

Mallory A. C., Reinhart B. J., Jones-Rhoades M. W., Tang G., Zamore P. D., Barton M. K., et al. . (2004). MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J. 23, 3356–3364. doi: 10.1038/sj.emboj.7600340 PubMed DOI PMC

Martin R. C., Mok M. C., Shaw G., Mok D. W. S. (1989). An enzyme mediating the conversion of zeatin to dihydrozeatin in phaseolus embryos. Plant Physiol. 90, 1630–1635. doi: 10.1104/pp.90.4.1630 PubMed DOI PMC

Mason M. G., Mathews D. E., Argyros D. A., Maxwell B. B., Kieber J. J., Alonso J. M., et al. . (2005). Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17, 3007–3018. doi: 10.1105/tpc.105.035451 PubMed DOI PMC

Mayer K. F. X., Schoof H., Haecker A., Lenhard M., Jürgens G., Laux T. (1998). Role of WUSCHEL in regulating stem cell fate in the arabidopsis shoot meristem. Cell 95, 805–815. doi: 10.1016/S0092-8674(00)81703-1 PubMed DOI

Meng W. J., Cheng Z. J., Sang Y. L., Zhang M. M., Rong X. F., Wang Z. W., et al. . (2017). Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL . Plant Cell 29, 1357–1372. doi: 10.1105/tpc.16.00640 PubMed DOI PMC

Miyawaki K., Tarkowski P., Matsumoto-Kitano M., Kato T., Sato S., Tarkowska D., et al. . (2006). Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 103, 16598–16603. doi: 10.1073/pnas.0603522103 PubMed DOI PMC

Moffatt B. A., Wang L., Allen M. S., Stevens Y. Y., Qin W., Snider J., et al. . (2000). Adenosine kinase of Arabidopsis. Kinetic properties and gene expression. Plant Physiol. 124, 1775–1785. doi: 10.1104/pp.124.4.1775 PubMed DOI PMC

Mor E., Pernisová M., Minne M., Cerutti G., Ripper D., Nolf J., et al. . (2022). bHLH heterodimer complex variations regulate cell proliferation activity in the meristems of Arabidopsis thaliana. iScience 25, 105364. doi: 10.1016/j.isci.2022.105364 PubMed DOI PMC

Nishimura C., Ohashi Y., Sato S., Kato T., Tabata S., Ueguchi C. (2004). Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in arabidopsis. Plant Cell 16, 1365–1377. doi: 10.1105/tpc.021477 PubMed DOI PMC

Ogawa M., Shinohara H., Sakagami Y., Matsubayashi Y. (2008). Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294–294. doi: 10.1126/science.1150083 PubMed DOI

Ohbayashi I., Sakamoto Y., Kuwae H., Kasahara H., Sugiyama M. (2022). Enhancement of shoot regeneration by treatment with inhibitors of auxin biosynthesis and transport during callus induction in tissue culture of Arabidopsis thaliana . Plant Biotechnol. 39, 43–50. doi: 10.5511/plantbiotechnology.21.1225a PubMed DOI PMC

Okushima Y., Fukaki H., Onoda M., Theologis A., Tasaka M. (2007). ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in arabidopsis . Plant Cell 19, 118–130. doi: 10.1105/tpc.106.047761 PubMed DOI PMC

Okushima Y., Overvoorde P. J., Arima K., Alonso J. M., Chan A., Chang C., et al. . (2005). Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in arabidopsis thaliana : unique and overlapping functions of ARF7 and ARF19 . Plant Cell 17, 444–463. doi: 10.1105/tpc.104.028316 PubMed DOI PMC

Osakabe Y., Miyata S., Urao T., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. (2002). Overexpression of Arabidopsis response regulators, ARR4/ATRR1/IBC7 and ARR8/ATRR3, alters cytokinin responses differentially in the shoot and in callus formation. Biochem. Biophys. Res. Commun. 293, 806–815. doi: 10.1016/S0006-291X(02)00286-3 PubMed DOI

Pernisova M., Grochova M., Konecny T., Plackova L., Harustiakova D., Kakimoto T., et al. . (2018). Cytokinin signalling regulates organ identity via the AHK4 receptor in Arabidopsis. Development 145, dev163907. doi: 10.1242/dev.163907 PubMed DOI

Pernisová M., Klíma P., Horák J., Válková M., Malbeck J., Souček P., et al. . (2009). Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proc. Natl. Acad. Sci. U.S.A. 106, 3609–3614. doi: 10.1073/pnas.0811539106 PubMed DOI PMC

Pernisová M., Kuderová A., Hejátko J. (2011). Cytokinin and auxin interactions in plant development: metabolism, signalling, transport and gene expression. Curr. Protein Pept. Sci. 12, 137–147. doi: 10.2174/138920311795684887 PubMed DOI

Pernisová M., Vernoux T. (2021). Auxin does the SAMba: auxin signaling in the shoot apical meristem. Cold Spring Harb. Perspect. Biol. 13, a039925. doi: 10.1101/cshperspect.a039925 PubMed DOI PMC

Pi L., Aichinger E., van der Graaff E., Llavata-Peris C. I., Weijers D., Hennig L., et al. . (2015). Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev. Cell 33, 576–588. doi: 10.1016/j.devcel.2015.04.024 PubMed DOI

Plong A., Rodriguez K., Alber M., Chen W., Reddy G. V. (2021). CLAVATA3 mediated simultaneous control of transcriptional and post-translational processes provides robustness to the WUSCHEL gradient. Nat. Commun. 12, 6361. doi: 10.1038/s41467-021-26586-0 PubMed DOI PMC

Qiao M., Xiang F. (2013). A set of Arabidopsis thaliana miRNAs involve shoot regeneration in vitro . Plant Signaling Behav. 8, e23479. doi: 10.4161/psb.23479 PubMed DOI PMC

Qiao M., Zhao Z., Song Y., Liu Z., Cao L., Yu Y., et al. . (2012). Proper regeneration from in vitro cultured Arabidopsis thaliana requires the microRNA-directed action of an auxin response factor: ARF10 in shoot regeneration in vitro . Plant J. 71, 14–22. doi: 10.1111/j.1365-313X.2012.04944.x PubMed DOI

Rashotte A. M., Mason M. G., Hutchison C. E., Ferreira F. J., Schaller G. E., Kieber J. J. (2006). A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc. Natl. Acad. Sci. U.S.A. 103, 11081–11085. doi: 10.1073/pnas.0602038103 PubMed DOI PMC

Reddy G. V., Heisler M. G., Ehrhardt D. W., Meyerowitz E. M. (2004). Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana . Development 131, 4225–4237. doi: 10.1242/dev.01261 PubMed DOI

Rodriguez K., Perales M., Snipes S., Yadav R. K., Diaz-Mendoza M., Reddy G. V. (2016). DNA-dependent homodimerization, sub-cellular partitioning, and protein destabilization control WUSCHEL levels and spatial patterning. Proc. Natl. Acad. Sci. U.S.A. 113, E6307–E6315. doi: 10.1073/pnas.1607673113 PubMed DOI PMC

Rosspopoff O., Chelysheva L., Saffar J., Lecorgne L., Gey D., Caillieux E., et al. . (2017). Direct conversion of root primordium into shoot meristem relies on timing of stem cell niche development. Development 144, 1187–1200. doi: 10.1242/dev.142570 PubMed DOI

Sakai H., Aoyama T., Oka A. (2000). Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 24, 703–711. doi: 10.1046/j.1365-313x.2000.00909.x PubMed DOI

Sarkar A. K., Luijten M., Miyashima S., Lenhard M., Hashimoto T., Nakajima K., et al. . (2007). Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811–814. doi: 10.1038/nature05703 PubMed DOI

Schaller G. E., Bishopp A., Kieber J. J. (2015). The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27, 44–63. doi: 10.1105/tpc.114.133595 PubMed DOI PMC

Schlereth A., Möller B., Liu W., Kientz M., Flipse J., Rademacher E. H., et al. . (2010). MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913–916. doi: 10.1038/nature08836 PubMed DOI

Schoof H., Lenhard M., Haecker A., Mayer K. F. X., Jürgens G., Laux T. (2000). The stem cell population of arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644. doi: 10.1016/S0092-8674(00)80700-X PubMed DOI

Schrumpfová P. P., Vychodilová I., Hapala J., Schořová Š., Dvořáček V., Fajkus J. (2016). Telomere binding protein TRB1 is associated with promoters of translation machinery genes in vivo . Plant Mol. Biol. 90, 189–206. doi: 10.1007/s11103-015-0409-8 PubMed DOI

Shim S., Lee H. G., Seo P. J. (2021). MET1-dependent DNA methylation represses light signaling and influences plant regeneration in arabidopsis . Mol. Cells 44, 746–757. doi: 10.14348/molcells.2021.0160 PubMed DOI PMC

Skoog F., Miller C. O. (1957). Chemical regulation of growth and organ formation in plant tissues cultured in vitro . Symp Soc. Exp. Biol. 54, 118–130. PubMed

Snipes S. A., Rodriguez K., DeVries A. E., Miyawaki K. N., Perales M., Xie M., et al. . (2018). Cytokinin stabilizes WUSCHEL by acting on the protein domains required for nuclear enrichment and transcription. PloS Genet. 14, e1007351. doi: 10.1371/journal.pgen.1007351 PubMed DOI PMC

Su Y. H., Zhou C., Li Y. J., Yu Y., Tang L. P., Zhang W. J., et al. . (2020). Integration of pluripotency pathways regulates stem cell maintenance in the Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. U.S.A. 117, 22561–22571. doi: 10.1073/pnas.2015248117 PubMed DOI PMC

Subban P., Kutsher Y., Evenor D., Belausov E., Zemach H., Faigenboim A., et al. . (2020). Shoot regeneration is not a single cell event. Plants 10, 58. doi: 10.3390/plants10010058 PubMed DOI PMC

Sugimoto K., Jiao Y., Meyerowitz E. M. (2010). Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev. Cell 18, 463–471. doi: 10.1016/j.devcel.2010.02.004 PubMed DOI

Suzuki T., Imamura A., Ueguchi C., Mizuno T. (1998). Histidine-containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol. 39, 1258–1268. doi: 10.1093/oxfordjournals.pcp.a029329 PubMed DOI

Takei K., Sakakibara H., Sugiyama T. (2001). Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J. Biol. Chem. 276, 26405–26410. doi: 10.1074/jbc.M102130200M102130200 PubMed DOI

Takei K., Yamaya T., Sakakibara H. (2004). Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-Zeatin. J. Biol. Chem. 279, 41866–41872. doi: 10.1074/jbc.M406337200 PubMed DOI

Tamaki H., Konishi M., Daimon Y., Aida M., Tasaka M., Sugiyama M. (2009). Identification of novel meristem factors involved in shoot regeneration through the analysis of temperature-sensitive mutants of Arabidopsis. Plant J. 57, 1027–1039. doi: 10.1111/j.1365-313X.2008.03750.x PubMed DOI

Tanaka Y., Suzuki T., Yamashino T., Mizuno T. (2004). Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 68, 462–465. doi: 10.1271/bbb.68.462 PubMed DOI

Temman H., Sakamoto T., Ueda M., Sugimoto K., Migihashi M., Yamamoto K., et al. . (2023). Histone deacetylation regulates de novo shoot regeneration. PNAS Nexus 2, pgad002. doi: 10.1093/pnasnexus/pgad002 PubMed DOI PMC

Temmerman A., Marquez-Garcia B., Depuydt S., Bruznican S., De Cuyper C., De Keyser A., et al. . (2022). MAX2 -dependent competence for callus formation and shoot regeneration from Arabidopsis thaliana root explants. J. Exp. Bot. 73, 6272–6291. doi: 10.1093/jxb/erac281 PubMed DOI

To J. P. C., Haberer G., Ferreira F. J., Deruère J., Mason M. G., Schaller G. E., et al. . (2004). Type-A arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling[W]. Plant Cell 16, 658–671. doi: 10.1105/tpc.018978 PubMed DOI PMC

Valvekens D., Montagu M. V., Lijsebettens M. V. (1988). Agrobacterium tumefaciens -mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl. Acad. Sci. U.S.A. 85, 5536–5540. doi: 10.1073/pnas.85.15.5536 PubMed DOI PMC

Varapparambath V., Mathew M. M., Shanmukhan A. P., Radhakrishnan D., Kareem A., Verma S., et al. . (2022). Mechanical conflict caused by a cell-wall-loosening enzyme activates de novo shoot regeneration. Dev. Cell 57, 2063–2080.e10. doi: 10.1016/j.devcel.2022.07.017 PubMed DOI

Vollbrecht E., Reiser L., Hake S. (2000). Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1 . Development 127, 3161–3172. doi: 10.1242/dev.127.14.3161 PubMed DOI

Wang L., Liu Z., Qiao M., Xiang F. (2018). miR393 inhibits in vitro shoot regeneration in Arabidopsis thaliana via repressing TIR1. Plant Sci. 266, 1–8. doi: 10.1016/j.plantsci.2017.10.009 PubMed DOI

Wang J., Tan M., Wang X., Jia L., Wang M., Huang A., et al. . (2023. a). WUS-RELATED HOMEOBOX 14 boosts de novo plant shoot regeneration. Plant Physiol. 192, 748–752. doi: 10.1093/plphys/kiad125 PubMed DOI PMC

Wang J.-W., Wang L.-J., Mao Y.-B., Cai W.-J., Xue H.-W., Chen X.-Y. (2005). Control of root cap formation by microRNA-targeted auxin response factors in arabidopsis. Plant Cell 17, 2204–2216. doi: 10.1105/tpc.105.033076 PubMed DOI PMC

Wang M., Zhong Z., Gallego-Bartolomé J., Feng S., Shih Y.-H., Liu M., et al. . (2023. b). Arabidopsis TRB proteins function in H3K4me3 demethylation by recruiting JMJ14. Nat. Commun. 14, 1736. doi: 10.1038/s41467-023-37263-9 PubMed DOI PMC

Weits D. A., Kunkowska A. B., Kamps N. C. W., Portz K. M. S., Packbier N. K., Nemec Venza Z., et al. . (2019). An apical hypoxic niche sets the pace of shoot meristem activity. Nature 569, 714–717. doi: 10.1038/s41586-019-1203-6 PubMed DOI

Xu M., Hu T., Zhao J., Park M.-Y., Earley K. W., Wu G., et al. . (2016). Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. PloS Genet. 12, e1006263. doi: 10.1371/journal.pgen.1006263 PubMed DOI PMC

Xue T., Dai X., Wang R., Wang J., Liu Z., Xiang F. (2017). ARGONAUTE10 Inhibits in vitro shoot regeneration via repression of miR165/166 in Arabidopsis thaliana. Plant Cell Physiol. 58, 1789–1800. doi: 10.1093/pcp/pcx117 PubMed DOI

Yadav R. K., Perales M., Gruel J., Girke T., Jönsson H., Reddy G. V. (2011). WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 25, 2025–2030. doi: 10.1101/gad.17258511 PubMed DOI PMC

Yamada M., Tanaka S., Miyazaki T., Aida M. (2022). Expression of the auxin biosynthetic genes YUCCA1 and YUCCA4 is dependent on the boundary regulators CUP-SHAPED COTYLEDON genes in the Arabidopsis thaliana embryo. Plant Biotechnol. 39, 37–42. doi: 10.5511/plantbiotechnology.21.0924a PubMed DOI PMC

Yan A., Borg M., Berger F., Chen Z. (2020). The atypical histone variant H3.15 promotes callus formation in Arabidopsis thaliana . Development 147, dev.184895. doi: 10.1242/dev.184895 PubMed DOI

Yanai O., Shani E., Dolezal K., Tarkowski P., Sablowski R., Sandberg G., et al. . (2005). Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15, 1566–1571. doi: 10.1016/j.cub.2005.07.060 PubMed DOI

Yang W., Choi M.-H., Noh B., Noh Y.-S. (2020). De novo shoot regeneration controlled by HEN1 and TCP3/4 in arabidopsis. Plant Cell Physiol. 61, 1600–1613. doi: 10.1093/pcp/pcaa083 PubMed DOI

Yang S., De Haan M., Mayer J., Janacek D. P., Hammes U. Z., Poppenberger B., et al. . (2022). A novel chemical inhibitor of polar auxin transport promotes shoot regeneration by local enhancement of HD-ZIP III transcription. New Phytol. 235, 1111–1128. doi: 10.1111/nph.18196 PubMed DOI

Yang B., Minne M., Brunoni F., Plačková L., Petřík I., Sun Y., et al. . (2021). Non-cell autonomous and spatiotemporal signalling from a tissue organizer orchestrates root vascular development. Nat. Plants 7, 1485–1494. doi: 10.1038/s41477-021-01017-6 PubMed DOI PMC

Yang S., Poretska O., Sieberer T. (2018). ALTERED MERISTEM PROGRAM1 restricts shoot meristem proliferation and regeneration by limiting HD-ZIP III-mediated expression of RAP2.6L. Plant Physiol. 177, 1580–1594. doi: 10.1104/pp.18.00252 PubMed DOI PMC

Zhai N., Xu L. (2021). Pluripotency acquisition in the middle cell layer of callus is required for organ regeneration. Nat. Plants 7, 1453–1460. doi: 10.1038/s41477-021-01015-8 PubMed DOI

Zhang T.-Q., Lian H., Tang H., Dolezal K., Zhou C.-M., Yu S., et al. . (2015). An intrinsic microRNA timer regulates progressive decline in shoot regenerative capacity in plants. Plant Cell 27, 349–360. doi: 10.1105/tpc.114.135186 PubMed DOI PMC

Zhang T.-Q., Lian H., Zhou C.-M., Xu L., Jiao Y., Wang J.-W. (2017. b). A Two-Step Model for de Novo Activation of WUSCHEL during Plant Shoot Regeneration. Plant Cell 29, 1073–1087. doi: 10.1105/tpc.16.00863 PubMed DOI PMC

Zhang F., May A., Irish V. F. (2017. a). Type-B ARABIDOPSIS RESPONSE REGULATORs directly activate WUSCHEL. Trends Plant Sci. 22, 815–817. doi: 10.1016/j.tplants.2017.08.007 PubMed DOI

Zhang S., Yu R., Yu D., Chang P., Guo S., Yang X., et al. . (2022). The calcium signaling module CaM–IQM destabilizes IAA–ARF interaction to regulate callus and lateral root formation. Proc. Natl. Acad. Sci. U.S.A. 119, e2202669119. doi: 10.1073/pnas.2202669119 PubMed DOI PMC

Zhang Z., Zhang X. (2012). Argonautes compete for miR165/166 to regulate shoot apical meristem development. Curr. Opin. Plant Biol. 15, 652–658. doi: 10.1016/j.pbi.2012.05.007 PubMed DOI PMC

Zhang M. M., Zhang H. K., Zhai J. F., Zhang X. S., Sang Y. L., Cheng Z. J. (2021). ARF4 regulates shoot regeneration through coordination with ARF5 and IAA12. Plant Cell Rep. 40, 315–325. doi: 10.1007/s00299-020-02633-w PubMed DOI

Zhao Z., Andersen S. U., Ljung K., Dolezal K., Miotk A., Schultheiss S. J., et al. . (2010). Hormonal control of the shoot stem-cell niche. Nature 465, 1089–1092. doi: 10.1038/nature09126 PubMed DOI

Zhou Y., Liu X., Engstrom E. M., Nimchuk Z. L., Pruneda-Paz J. L., Tarr P. T., et al. . (2015). Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 517, 377–380. doi: 10.1038/nature13853 PubMed DOI PMC

Zhou Y., Wang Y., Krause K., Yang T., Dongus J. A., Zhang Y., et al. . (2018. a). Telobox motifs recruit CLF/SWN–PRC2 for H3K27me3 deposition via TRB factors in Arabidopsis. Nat. Genet. 50, 638–644. doi: 10.1038/s41588-018-0109-9 PubMed DOI

Zhou Y., Yan A., Han H., Li T., Geng Y., Liu X., et al. . (2018. b). HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers. Science 361, 502–506. doi: 10.1126/science.aar8638 PubMed DOI PMC

Zubo Y. O., Blakley I. C., Yamburenko M. V., Worthen J. M., Street I. H., Franco-Zorrilla J. M., et al. . (2017). Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in Arabidopsis . Proc. Natl. Acad. Sci. U.S.A. 114, E5995–E6004. doi: 10.1073/pnas.1620749114 PubMed DOI PMC

Epigenetics and plant hormone dynamics: a functional and methodological perspective