Integrating the Roles for Cytokinin and Auxin in De Novo Shoot Organogenesis: From Hormone Uptake to Signaling Outputs

. 2021 Aug 09 ; 22 (16) : . [epub] 20210809

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid34445260

Grantová podpora
451-03-9/2021-14/200007 Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
19-13103S Grantová Agentura České Republiky

De novo shoot organogenesis (DNSO) is a procedure commonly used for the in vitro regeneration of shoots from a variety of plant tissues. Shoot regeneration occurs on nutrient media supplemented with the plant hormones cytokinin (CK) and auxin, which play essential roles in this process, and genes involved in their signaling cascades act as master regulators of the different phases of shoot regeneration. In the last 20 years, the genetic regulation of DNSO has been characterized in detail. However, as of today, the CK and auxin signaling events associated with shoot regeneration are often interpreted as a consequence of these hormones simply being present in the regeneration media, whereas the roles for their prior uptake and transport into the cultivated plant tissues are generally overlooked. Additionally, sucrose, commonly added to the regeneration media as a carbon source, plays a signaling role and has been recently shown to interact with CK and auxin and to affect the efficiency of shoot regeneration. In this review, we provide an integrative interpretation of the roles for CK and auxin in the process of DNSO, adding emphasis on their uptake from the regeneration media and their interaction with sucrose present in the media to their complex signaling outputs that mediate shoot regeneration.

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Yildiz M. The prerequisite of the success in plant tissue culture: High frequency shoot regeneration. In: Leva A., Rinaldi L.M.R., editors. Recent Advances in Plant In Vitro Culture. IntechOpen Limited; London, UK: 2012. pp. 63–90.

Hill K., Schaller G.E. Enhancing plant regeneration in tissue culture. Plant Signal. Behav. 2013;8:e25709. doi: 10.4161/psb.25709. PubMed DOI PMC

Ckurshumova W., Berleth T. Overcoming recalcitrance—Auxin response factor functions in plant regeneration. Plant Signal. Behav. 2015;10:e993293. doi: 10.4161/15592324.2014.993293. PubMed DOI PMC

Motte H., Vereecke D., Geelen D., Werbrouck S. The molecular path to in vitro shoot regeneration. Biotechnol. Adv. 2014;32:107–121. doi: 10.1016/j.biotechadv.2013.12.002. PubMed DOI

Ikeuchi M., Ogawa Y., Iwase A., Sugimoto K. Plant regeneration: Cellular origins and molecular mechanisms. Development. 2016;143:1442–1451. doi: 10.1242/dev.134668. PubMed DOI

Kareem A., Radhakrishnan D., Sondhi Y., Aiyaz M., Roy M.V., Sugimoto K., Prasad K. De novo assembly of plant body plan: A step ahead of deadpool. Regeneration. 2016;3:182–197. doi: 10.1002/reg2.68. PubMed DOI PMC

Radhakrishnan D., Kareem A., Durgaprasad K., Sreeraj E., Sugimoto K., Prasad K. Shoot regeneration: A journey from acquisition of competence to completion. Curr. Opin. Plant Biol. 2018;41:23–31. doi: 10.1016/j.pbi.2017.08.001. PubMed DOI

Tian X., Zhang C., Xu J. Control of cell fate reprogramming towards de novo shoot organogenesis. Plant Cell Physiol. 2018;59:713–719. doi: 10.1093/pcp/pcx207. PubMed DOI

Ikeuchi M., Favero D.S., Sakamoto Y., Iwase A., Coleman D., Rymen B., Sugimoto K. Molecular mechanisms of plant regeneration. Annu. Rev. Plant Biol. 2019;70:377–406. doi: 10.1146/annurev-arplant-050718-100434. PubMed DOI

Sugimoto K., Temman H., Kadokura S., Matsunaga S. To regenerate or not to regenerate: Factors that drive plant regeneration. Curr. Opin. Plant Biol. 2019;47:138–150. doi: 10.1016/j.pbi.2018.12.002. PubMed DOI

Shin J., Bae S., Seo P.J. De novo shoot organogenesis during plant regeneration. J. Exp. Bot. 2020;71:63–72. doi: 10.1093/jxb/erz395. PubMed DOI

Hnatuszko-Konka K., Gerszberg A., Weremczuk-Jeżyna I., Grzegorczyk-Karolak I. Cytokinin signaling and de novo shoot organogenesis. Genes. 2021;12:265. doi: 10.3390/genes12020265. PubMed DOI PMC

Skoog F., Miller C.O. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 1957;11:118–130. PubMed

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

Che P., Gingerich D.J., Lall S., Howell S.H. Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell. 2002;14:2771–2785. doi: 10.1105/tpc.006668. PubMed DOI PMC

Cary A.J., Che P., Howell S.H. Developmental events and shoot apical meristem gene expression patterns during shoot development in Arabidopsis thaliana. Plant J. 2002;32:867–877. doi: 10.1046/j.1365-313X.2002.01479.x. PubMed DOI

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

Ikeuchi M., Sugimoto K., Iwase A. Plant callus: Mechanisms of induction and repression. Plant Cell. 2013;25:3159–3173. doi: 10.1105/tpc.113.116053. PubMed DOI PMC

Fehér A. Callus, dedifferentiation, totipotency, somatic embryogenesis: What these terms mean in the era of molecular plant biology? Front. Plant Sci. 2019;10:536. doi: 10.3389/fpls.2019.00536. PubMed DOI PMC

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

Ikeuchi M., Shibata M., Rymen B., Iwase A., Bågman A.M., Watt L., Coleman D., Favero D.S., Takahashi T., Ahnert S.E., et al. A gene regulatory network for cellular reprogramming in plant regeneration. Plant Cell Physiol. 2018;59:770–782. doi: 10.1093/pcp/pcy013. PubMed DOI PMC

Alvarez J.M., Bueno N., Cuesta C., Feito I., Ordás R.J. Hormonal and gene dynamics in de novo shoot meristem formation during adventitious caulogenesis in cotyledons of Pinus pinea. Plant Cell Rep. 2020;39:527–541. doi: 10.1007/s00299-020-02508-0. PubMed DOI PMC

Muñoz A., Mangano S., González-García M.P., Contreras R., Sauer M., De Rybel B., Weijers D., Sánchez-Serrano J.J., Sanmartín M., Rojo E. RIMA-dependent nuclear accumulation of IYO triggers auxin-irreversible cell differentiation in arabidopsis. Plant Cell. 2017;29:575–588. doi: 10.1105/tpc.16.00791. PubMed DOI PMC

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

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

Torres-Martínez H.H., Rodríguez-Alonso G., Shishkova S., Dubrovsky J.G. Lateral root primordium morphogenesis in angiosperms. Front. Plant Sci. 2019;10:206. doi: 10.3389/fpls.2019.00206. PubMed DOI PMC

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

Pernisova M., Grochova M., Konecny T., Plackova L., Harustiakova D., Kakimoto T., Heisler M.G., Novak O., Hejatko J. Cytokinin signalling regulates organ identity via the AHK4 receptor in arabidopsis. Development. 2018;145:dev163907. doi: 10.1242/dev.163907. PubMed DOI

Ćosić T., Raspor M., Savić J., Cingel A., Matekalo D., Zdravković-Korać S., Ninković S. Expression profiles of organogenesis-related genes over the time course of one-step de novo shoot organogenesis from intact seedlings of kohlrabi. J. Plant Physiol. 2019;232:257–269. doi: 10.1016/j.jplph.2018.11.004. PubMed DOI

Lee M.H., Lee J., Jie E.Y., Choi S.H., Jiang L., Ahn W.S., Kim C.Y., Kim S.W. Temporal and spatial expression analysis of shoot-regeneration regulatory genes during the adventitious shoot formation in hypocotyl and cotyledon explants of tomato (cv. Micro-Tom) Int. J. Mol. Sci. 2020;21:5309. doi: 10.3390/ijms21155309. PubMed DOI PMC

Kakani A., Li G., Peng Z. Role of AUX1 in the control of organ identity during in vitro organogenesis and in mediating tissue specific auxin and cytokinin interaction in arabidopsis. Planta. 2009;229:645–657. doi: 10.1007/s00425-008-0846-6. PubMed DOI

Hu W., Fagundez S., Katin-Grazzini L., Li Y., Li W., Chen Y., Wang X., Deng Z., Xie S., McAvoy R.J., et al. Endogenous auxin and its manipulation influence in vitro shoot organogenesis of citrus epicotyl explants. Hortic. Res. 2017;4:17071. doi: 10.1038/hortres.2017.71. PubMed DOI PMC

Benková E., Michniewicz M., Sauer M., Teichmann T., Seifertová D., Jürgens G., Friml J. Local, efflux-dependent auxin gradient as a common module for plant organ formation. Cell. 2003;115:591–602. doi: 10.1016/S0092-8674(03)00924-3. PubMed DOI

Swarup R., Péret B. AUX/LAX family of auxin influx carriers—An overview. Front. Plant Sci. 2012;3:225. doi: 10.3389/fpls.2012.00225. PubMed DOI PMC

Pernisová M., Klíma P., Horák J., Válková M., Malbeck J., Souček P., Reichman P., Hoyerová K., Dubová J., Friml J., et al. Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proc. Natl. Acad. Sci. USA. 2009;106:3609–3614. doi: 10.1073/pnas.0811539106. PubMed DOI PMC

Marhavý P., Vanstraelen M., De Rybel B., Zhaojun D., Bennett M.J., Beeckman T., Benková E. Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J. 2013;32:149–158. doi: 10.1038/emboj.2012.303. PubMed DOI PMC

Krogan N.T., Marcos D., Weiner A.I., Berleth T. The auxin response factor MONOPTEROS controls meristem function and organogenesis in both the shoot and root through the direct regulation of PIN genes. New Phytol. 2016;212:42–50. doi: 10.1111/nph.14107. PubMed DOI PMC

De Rybel B., Vassileva V., Parizot B., Demeulenaere M., Grunewald W., Audenaert D., Van Campenhout J., Overvoorde P., Jansen L., Vanneste S., et al. A Novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol. 2010;20:1697–1706. doi: 10.1016/j.cub.2010.09.007. PubMed DOI

Olmo R., Cabrera J., Díaz-Manzano F.E., Ruiz-Ferrer V., Barcala M., Ishida T., García A., Andrés M.F., Ruiz-Lara S., Verdugo I., et al. Root-knot nematodes induce gall formation by recruiting developmental pathways of post-embryonic organogenesis and regeneration to promote transient pluripotency. New Phytol. 2020;227:200–215. doi: 10.1111/nph.16521. PubMed DOI

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

Okushima Y., Overvoorde P.J., Arima K., Alonso J.M., Chan A., Chang C., Ecker J.R., Hughes B., Lui A., Nguyen D., et al. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: Unique and overlapping functions of ARF7 and ARF19. Plant Cell. 2005;17:444–463. doi: 10.1105/tpc.104.028316. PubMed DOI PMC

Fukaki H., Nakao Y., Okushima Y., Theologis A., Tasaka M. Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in arabisopsis. Plant J. 2005;44:382–395. doi: 10.1111/j.1365-313X.2005.02537.x. PubMed DOI

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

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

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. Auxin-dependent cell cycle reactivation through transcriptional regulation of arabidopsis E2Fa by LATERAL ORGAN BOUNDARY proteins. Plant Cell. 2011;23:3671–3683. doi: 10.1105/tpc.111.088377. PubMed DOI PMC

Fan M., Xu C., Xu K., Hu Y. Lateral organs boundary domain transcription factors direct callus formation in arabidopsis regeneration. Cell Res. 2012;22:1169–1180. doi: 10.1038/cr.2012.63. PubMed DOI PMC

Lee K., Seo P.J. Arabidopsis TOR signaling is essential for sugar-regulated callus formation. J. Integr. Plant Biol. 2017;59:742–746. doi: 10.1111/jipb.12560. PubMed DOI

Xu C., Cao H., Xu E., Zhang S., Hu Y. Genome-wide identification of arabidopsis LBD29 target genes reveals the molecular events behind auxin-induced cell reprogramming during callus formation. Plant Cell. Physiol. 2018;59:749–760. doi: 10.1093/pcp/pcx168. PubMed DOI

Xu C., Cao H., Zhang Q., Wang H., Xin W., Xu E., Zhang S., Yu R., Yu D., Hu Y. Control of auxin-induced callus formation by bZIP59-LBD complex in arabidopsis regeneration. Nat. Plants. 2018;4:108–115. doi: 10.1038/s41477-017-0095-4. PubMed DOI

Sheng L., Hu X., Du Y., Zhang G., Huang H., Scheres B., Xu L. Non-Canonical WOX11-mediated root branching contributes to plasticity in arabidopsis root system architecture. Development. 2017;144:3126–3133. PubMed PMC

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

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

Sarkar A.K., Luijten M., Miyashima S., Lenhard M., Hashimoto T., Nakajima K., Scheres B., Heidstra R., Laux T. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature. 2007;446:811–814. doi: 10.1038/nature05703. PubMed DOI

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

García-Gómez M.L., Azpeitia E., Álvarez-Buylla E.R. A Dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana. PLoS Comput. Biol. 2017;13:e1005488. doi: 10.1371/journal.pcbi.1005488. PubMed DOI PMC

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

Salvi E., Di Mambro R., Pacifici E., Dello Ioio R., Costantino P., Moubayidin L., Sabatini S. SCARECROW and SHORTROOT control the auxin/cytokinin balance necessary for embryonic stem cell niche specification. Plant Signal. Behav. 2018;13:e1507402. PubMed PMC

Horstman A., Willemsen V., Boutilier K., Heidstra R. Aintegumenta-like proteins: Hubs in a plethora of networks. Trends Plant Sci. 2014;19:146–157. doi: 10.1016/j.tplants.2013.10.010. PubMed DOI

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., et al. The PLETHORA gene regulatory network guides growth and cell differentiation in arabidopsis roots. Plant Cell. 2016;28:2937–2951. doi: 10.1105/tpc.16.00656. PubMed DOI PMC

Kareem A., Durgaprasad K., Sugimoto K., Du Y., Pulianmackal A.J., Trivedi Z.B., Abhayadev P.V., Pinon V., Meyerowitz E.M., Scheres B., et al. PLETHORA genes control regeneration by a two-step mechanism. Curr. Biol. 2015;25:1017–1030. doi: 10.1016/j.cub.2015.02.022. PubMed DOI PMC

Iwase A., Mitsuda N., Koyama T., Hiratsu K., Kojima M., Arai T., Inoue Y., Seki M., Sakakibara H., Sugimoto K., et al. The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in arabidopsis. Curr. Biol. 2011;21:508–514. doi: 10.1016/j.cub.2011.02.020. PubMed DOI

Ikeuchi M., Iwase A., Rymen B., Lambolez A., Kojima M., Takebayashi Y., Heyman J., Watanabe S., Seo M., De Veylder L., et al. Wounding triggers callus formation via dynamic hormonal and transcriptional changes. Plant Physiol. 2017;175:1158–1174. doi: 10.1104/pp.17.01035. PubMed DOI PMC

Iwase A., Harashima H., Ikeuchi M., Rymen B., Ohnuma M., Komaki S., Morohashi K., Kurata T., Nakata M., Ohme-Takagi M., et al. WIND1 promotes shoot regeneration through transcriptional activation of ENHANCER OF SHOOT REGENERATION1 in arabidopsis. Plant Cell. 2017;29:54–69. doi: 10.1105/tpc.16.00623. PubMed DOI PMC

Motte H., Vercauteren A., Depuydt S., Landschoot S., Geelen D., Werbrouck S., Goormachtig S., Vuylsteke M., Vereecke D. Combining linkage and association mapping identifies RECEPTOR-LIKE PROTEIN KINASE1 as an essential arabidopsis shoot regeneration gene. Proc. Natl. Acad. Sci. USA. 2014;111:8305–8310. doi: 10.1073/pnas.1404978111. PubMed DOI PMC

Banno H., Ikeda Y., Niu Q.W., Chua N.H. Overexpression of arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell. 2001;13:2609–2618. doi: 10.1105/tpc.010234. PubMed DOI PMC

Kirch T., Simon R., Grünewald M., Werr W. The DORNRÖSCHEN/ENHANCER OF SHOOT REGENERATION1 Gene of Arabidopsis acts in the control of meristem cell fate and lateral organ development. Plant Cell. 2003;15:694–705. doi: 10.1105/tpc.009480. PubMed DOI PMC

Luo L., Zeng J., Wu H., Tian Z., Zhao Z. A molecular framework for auxin-controlled homeostasis of shoot stem cells in arabidopsis. Mol. Plant. 2018;11:899–913. doi: 10.1016/j.molp.2018.04.006. PubMed DOI

Matsuo N., Makino M., Banno H. Arabidopsis ENHANCER OF SHOOT REGENERATION (ESR)1 and ESR2 regulate in vitro shoot regeneration and their expressions are differently regulated. Plant Sci. 2011;181:39–46. doi: 10.1016/j.plantsci.2011.03.007. PubMed DOI

Ikeda Y., Banno H., Niu Q.W., Howell S.H., Chua N.H. The ENHANCER OF SHOOT REGENERATION 2 gene in Arabidopsis regulates CUP-SHAPED COTYLEDON 1 at the transcriptional level and controls cotyledon development. Plant Cell Physiol. 2006;47:1443–1456. doi: 10.1093/pcp/pcl023. PubMed DOI

Matsuo N., Mase H., Makino M., Takahashi H., Banno H. Identification of ENHANCER OF SHOOT REGENERATION 1-upregulated genes during in vitro shoot regeneration. Plant Biotechnol. 2009;26:385–393. doi: 10.5511/plantbiotechnology.26.385. DOI

Seeliger I., Frerichs A., Glowa D., Velo L., Comelli P., Chandler J.W., Werr W. The AP2-type transcription factors DORNRÖSCHEN and DORNRÖSCHEN-LIKE promote G1/S transition. Mol. Genet. Genom. 2016;291:1835–1849. doi: 10.1007/s00438-016-1224-x. PubMed DOI

Aida M., Ishida T., Fukaki H., Fujisawa H., Tasaka M. Genes involved in organ separation in arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell. 1997;9:841–857. doi: 10.1105/tpc.9.6.841. PubMed DOI PMC

Vroemen C.W., Mordhorst A.P., Albrecht C., Kwaaitaal M.A.C.J., de Vries S.C. The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in arabidopsis. Plant Cell. 2003;15:1563–1577. doi: 10.1105/tpc.012203. PubMed DOI PMC

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

Hibara K., Karim M.R., Takada S., Taoka K., Furutani M., Aida M., Tasaka M. Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell. 2006;18:2946–2957. doi: 10.1105/tpc.106.045716. PubMed DOI PMC

Takada S., Hibara K., Ishida T., Tasaka M. The CUP-SHAPED COTYLEDON1 gene of arabidopsis regulates shoot apical meristem formation. Development. 2001;128:1127–1135. doi: 10.1242/dev.128.7.1127. PubMed DOI

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

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

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

Traas J. Organogenesis at the shoot apical meristem. Plants. 2019;8:6. doi: 10.3390/plants8010006. PubMed DOI PMC

Rupp H.M., Frank M., Werner T., Strnad M., Schmülling T. Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem. Plant J. 1999;18:557–563. doi: 10.1046/j.1365-313X.1999.00472.x. PubMed DOI

Jasinski S., Piazza P., Craft J., Hay A., Woolley L., Rieu I., Phillips A., Hedden P., Tsiantis M. KNOX Action in arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 2005;15:1560–1565. doi: 10.1016/j.cub.2005.07.023. PubMed DOI

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

Chung Y., Zhu Y., Wu M.F., Simonini S., Kuhn A., Armenta-Medina A., Jin R., Østergaard L., Stewart G.C., Wagner D. Auxin response factors promote organogenesis by chromatin-mediated repression of the pluripotency gene SHOOTMERISTEMLESS. Nat. Commun. 2019;10:886. doi: 10.1038/s41467-019-08861-3. PubMed DOI PMC

Zhao Q.H., Fisher R., Auer C. Developmental phases and STM expression during arabidopsis shoot organogenesis. Plant Growth Regul. 2002;37:223–231. doi: 10.1023/A:1020838712634. DOI

Wang Q., Hasson A., Rossmann S., Theres K. Divide Et Impera: Boundaries shape the plant body and initiate new meristems. New Phytol. 2016;209:485–498. doi: 10.1111/nph.13641. PubMed DOI

Landrein B., Kiss A., Sassi M., Chauvet A., Das P., Cortizo M., Laufs P., Takeda S., Aida M., Traas J., et al. Mechanical stress contributes to the expression of the STM homeobox gene in arabidopsis shoot meristems. eLife. 2015;4:e07811. doi: 10.7554/eLife.07811. PubMed DOI PMC

Fal K., Landrein B., Hamant O. Interplay between miRNA regulation and mechanical stress for CUC gene expression at the shoot apical meristem. Plant Signal. Behav. 2016;11:e1127497. doi: 10.1080/15592324.2015.1127497. PubMed DOI PMC

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

Dolzblasz A., Nardmann J., Clerici E., Causier B., van der Graaff E., Chen J., Davies B., Werr W., Laux T. Stem Cell Regulation by arabidopsis WOX genes. Mol. Plant. 2016;9:1028–1039. doi: 10.1016/j.molp.2016.04.007. PubMed DOI

Tvorogova V.E., Krasnoperova E.Y., Potsenkovskaia E.A., Kudriashov A.A., Dodueva I.E., Lutova L.A. What does the WOX say? Review of regulators, targets, partners. Mol. Biol. 2021;3:1–27. doi: 10.1134/S002689332102031X. PubMed DOI

Wu C.C., Li F.W., Kramer E.M. Large-scale phylogenomic analysis suggests three ancient superclades of the WUSCHEL-RELATED HOMEOBOX transcription factor family in plants. PLoS ONE. 2019;14:e0223521. doi: 10.1371/journal.pone.0223521. PubMed DOI PMC

Endrizzi K., Moussian B., Haecker A., Levin J.Z., Laux T. The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J. 1996;10:967–979. doi: 10.1046/j.1365-313X.1996.10060967.x. PubMed DOI

Lenhard M., Jürgens G., Laux T. The WUSCHEL and SHOOTMERISTEMLESS genes fulfill complementary roles in arabidopsis shoot meristem regulation. Development. 2002;129:3195–3206. doi: 10.1242/dev.129.13.3195. PubMed DOI

Ma Y., Miotk A., Šutiković Z., Ermakova O., Wenzl C., Medzihradszky A., Gaillochet C., Forner J., Utan G., Brackmann K., et al. WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in arabidopsis. Nat. Commun. 2019;10:5093. doi: 10.1038/s41467-019-13074-9. PubMed DOI PMC

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

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

Brand U., Fletcher J.C., Hobe M., Meyerowitz E.M., Simon R. Dependence of stem cell fate in arabidopsis on a feedback loop regulated by CLV3 activity. Science. 2000;289:617–619. doi: 10.1126/science.289.5479.617. PubMed DOI

Perales M., Rodriguez K., Snipes S., Yadav R.K., Diaz-Mendoza M., Reddy G.V. Threshold-dependent transcriptional discrimination underlies stem cell homeostasis. Proc. Natl. Acad. Sci. USA. 2016;113:6298–6306. doi: 10.1073/pnas.1607669113. PubMed DOI PMC

Somssich M., Je B.I., Simon R., Jackson D. CLAVATA-WUSCHEL signaling in the shoot meristem. Development. 2016;143:3238–3248. doi: 10.1242/dev.133645. PubMed DOI

Adibi M., Yoshida S., Weijers D., Fleck C. Centering the organizing center in the Arabidopsis thaliana shoot apical meristem by a combination of cytokinin signaling and self-organization. PLoS ONE. 2016;11:e0147830. doi: 10.1371/journal.pone.0147830. PubMed DOI PMC

Zhang T.Q., Lian H., Zhou C.M., Xu L., Jiao Y., Wang J.W. A two-step model for de novo activation of WUSCHEL during plant shoot regeneration. Plant Cell. 2017;29:1073–1087. doi: 10.1105/tpc.16.00863. PubMed DOI PMC

Zubo Y.O., Blakley I.C., Yamburenko M.V., Worthen J.M., Street I.H., Franco-Zorrilla J.M., Zhang W., Hill K., Raines T., Solano R., et al. Cytokinin induces genome-wide binding of the type-b response regulator ARR10 to regulate growth and development in arabidopsis. Proc. Natl. Acad. Sci. USA. 2017;114:5995–6004. doi: 10.1073/pnas.1620749114. PubMed DOI PMC

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

Wang J., Tian C., Zhang C., Shi B., Cao X., Zhang T.Q., Zhao Z., Wang J.W., Jiao Y. Cytokinin signaling activates WUSCHEL expression during axillary meristem initiation. Plant Cell. 2017;29:1373–1387. doi: 10.1105/tpc.16.00579. PubMed DOI PMC

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

Liu X., Dinh T.T., Li D., Shi B., Li Y., Cao X., Guo L., Pan Y., Jiao Y., Chen X. AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA2 in floral meristem determinacy. Plant J. 2014;80:629–641. doi: 10.1111/tpj.12658. PubMed DOI PMC

Ćosić T., Motyka V., Raspor M., Savić J., Cingel A., Vinterhalter B., Vinterhalter D., Trávničková A., Dobrev P.I., Bohanec B., et al. In vitro shoot organogenesis and comparative analysis of endogenous phytohormones in kohlrabi (Brassica oleracea var. gongylodes): Effects of genotype, explant type and applied cytokinins. Plant Cell Tissue Organ Cult. 2015;121:741–760. doi: 10.1007/s11240-015-0742-2. DOI

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

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

Xie M., Chen H., Huang L., O’Neil R.C., Shokhirev M.N., Ecker J.R. A B-ARR-mediated cytokinin transcriptional network directs hormone cross-regulation and shoot development. Nat. Commun. 2018;9:1604. doi: 10.1038/s41467-018-03921-6. PubMed DOI PMC

Zhang Z., Tucker E., Hermann M., Laux T. A molecular framework for the embryonic initiation of shoot meristem stem cells. Dev. Cell. 2017;40:264–277. doi: 10.1016/j.devcel.2017.01.002. PubMed DOI

Chung K.M., Sakamoto S., Mitsuda N., Suzuki K., Ohme-Takagi M., Fujiwara S. WUSCHEL-RELATED HOMEOBOX 2 is a transcriptional repressor involved in lateral organ formation and separation in arabidopsis. Plant Biotechnol. 2016;33:245–253. doi: 10.5511/plantbiotechnology.16.0202a. PubMed DOI PMC

Kyo M., Maida K., Nishioka Y., Matsui K. Coexpression of WUSCHEL Related Homeobox (WOX) 2 with WOX8 or WOX9 promotes regeneration from leaf segments and free cells in Nicotiana tabacum L. Plant Biotechnol. 2018;35:23–30. doi: 10.5511/plantbiotechnology.18.0126a. PubMed DOI PMC

Wang H., Niu L., Fu C., Meng Y., Sang D., Yin P., Wu J., Tang Y., Lu T., Wang Z.Y., et al. Overexpression of the WOX gene STENOFOLIA improves biomass yield and sugar release in transgenic grasses and display altered cytokinin homeostasis. PLoS Genet. 2017;13:e1006649. doi: 10.1371/journal.pgen.1006649. PubMed DOI PMC

Desjardins Y., Hdider C., de Riek J. Carbon nutrition in vitro—Regulation and manipulation of carbon assimilation in micropropagated systems. In: Aitken-Christie J., Kozai T., Smith M.A.L., editors. Automation and Environmental Control in Plant Tissue Culture. Springer Nature; Cham, Switzerland: 1995. pp. 441–471.

Huang W.L., Liu L.F. Carbohydrate Metabolism in rice during callus induction and shoot regeneration induced by osmotic stress. Bot. Bull. Acad. Sin. 2002;43:107–113.

Lee S.T., Huang W.L. Cytokinin, auxin, and abscisic acid affects sucrose metabolism conduce to de novo shoot organogenesis in rice (Oryza sativa L.) callus. Bot. Stud. 2013;54:5. doi: 10.1186/1999-3110-54-5. PubMed DOI PMC

Gibson S.I. Control of plant development and gene expression by sugar signaling. Curr. Opin. Plant Biol. 2005;8:93–102. doi: 10.1016/j.pbi.2004.11.003. PubMed DOI

Wang M., Le Gourrierec J., Jiao F., Demotes-Mainard S., Perez-Garcia M.D., Ogé L., Hamama L., Crespel L., Bertheloot J., Chen J., et al. Convergence and divergence of sugar and cytokinin signaling in plant development. Int. J. Mol. Sci. 2021;22:1282. doi: 10.3390/ijms22031282. PubMed DOI PMC

Sami F., Yusuf M., Faizan M., Faraz A., Hayat S. Role of sugars under abiotic stress. Plant Physiol. Biochem. 2016;109:54–61. doi: 10.1016/j.plaphy.2016.09.005. PubMed DOI

Chen J.G., Willard F.S., Huang J., Liang J., Chasse S.A., Jones A.M., Siderovski D.P. A seven-transmembrane RGS protein that modulates plant cell proliferation. Science. 2003;301:1728–1731. doi: 10.1126/science.1087790. PubMed DOI

Kushwah S., Laxmi A. The interaction between glucose and cytokinin signaling in controlling Arabidopsis thaliana seedling root growth and development. Plant Signal. Behav. 2017;12:e1312241. doi: 10.1080/15592324.2017.1312241. PubMed DOI PMC

Sakr S., Wang M., Dédaldéchamp F., Perez-Garcia M.D., Ogé L., Hamama L., Atanassova R. The sugar-signaling hub: Overview of regulators and interaction with the hormonal and metabolic network. Int. J. Mol. Sci. 2018;19:2506. doi: 10.3390/ijms19092506. PubMed DOI PMC

Kotov A.A., Kotova L.M., Romanov G.A. Signaling Network regulating plant branching: Recent advances and new challenges. Plant Sci. 2021;307:110880. doi: 10.1016/j.plantsci.2021.110880. PubMed DOI

Stewart J.L., Maloof J.N., Nemhauser J.L. PIF genes mediate the effect of sucrose on seedling growth dynamics. PLoS ONE. 2011;6:e19894. doi: 10.1371/journal.pone.0019894. PubMed DOI PMC

Sairanen I., Novák O., Pĕnčík A., Ikeda Y., Jones B., Sandberg G., Ljung K. Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in arabidopsis. Plant Cell. 2012;24:4907–4916. doi: 10.1105/tpc.112.104794. PubMed DOI PMC

Stewart Lilley J.L., Gee C.W., Sairanen I., Ljung K., Nemhauser J.L. An Endogenous carbon-sensing pathway triggers increased auxin flux and hypocotyl elongation. Plant Physiol. 2012;160:2261–2270. doi: 10.1104/pp.112.205575. PubMed DOI PMC

Sagar M., Chervin C., Roustan J.P., Bouzayen M., Zouine M. Under-expression of the auxin response factor Sl-ARF4 improves postharvest behavior of tomato fruits. Plant Signal. Behav. 2013;8:e25647. doi: 10.4161/psb.25647. PubMed DOI PMC

Kong D., Hao Y., Cui H. The WUSCHEL related homeobox protein WOX7 Regulates the sugar response of lateral root development in Arabidopsis thaliana. Mol. Plant. 2016;9:261–270. doi: 10.1016/j.molp.2015.11.006. PubMed DOI

Kushwah S., Laxmi A. The interaction between glucose and cytokinin signal transduction pathway in Arabidopsis thaliana. Plant Cell Environ. 2014;37:235–253. doi: 10.1111/pce.12149. PubMed DOI

Riou-Khamlichi C., Huntley R., Jacqmard A., Murray J.A.H. Cytokinin activation of arabidopsis cell division through a D-Type cyclin. Science. 1999;283:1541–1544. doi: 10.1126/science.283.5407.1541. PubMed DOI

Riou-Khamlichi C., Menges M., Healy J.M.S., Murray J.A.H. Sugar control of the plant cell cycle: Differential regulation of arabidopsis D-Type cyclin gene expression. Mol. Cell. Biol. 2000;20:4513–4521. doi: 10.1128/MCB.20.13.4513-4521.2000. PubMed DOI PMC

Hartig K., Beck E. Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biol. 2006;8:389–396. doi: 10.1055/s-2006-923797. PubMed DOI

Kiba T., Takebayashi Y., Kojima M., Sakakibara H. Sugar-induced de novo cytokinin biosynthesis contributes to arabidopsis growth under elevated CO2. Sci. Rep. 2019;9:7765. doi: 10.1038/s41598-019-44185-4. PubMed DOI PMC

Stokes M.E., Chattopadhyay A., Wilkins O., Nambara E., Campbell M.M. Interplay between sucrose and folate modulates auxin signaling in arabidopsis. Plant Physiol. 2013;162:1552–1565. doi: 10.1104/pp.113.215095. PubMed DOI PMC

Ho W.J., Vasil I.K. Somatic embryogenesis in sugarcane (Saccharum officinarum L.): Growth and plant regeneration from embryogenic cell suspension cultures. Ann. Bot. 1983;51:719–726. doi: 10.1093/oxfordjournals.aob.a086523. DOI

Thorpe T.A., Joy R.W., Leung D.W.M. Starch turnover in shoot-forming tobacco callus. Physiol. Plant. 1986;66:58–62. doi: 10.1111/j.1399-3054.1986.tb01233.x. DOI

Mangat B.S., Pelekis M.K., Cassells A.C. Changes in the starch content during organogenesis in in vitro cultured Begonia rex stem explants. Physiol. Plant. 1990;79:267–274. doi: 10.1111/j.1399-3054.1990.tb06741.x. DOI

Huang W.L., Wang Y.C., Lee P.D., Liu L.F. The regenerability of rice callus is closely related to starch metabolism. Taiwan. J. Agric. Chem. Food Sci. 2006;44:100–107.

Kumari A., Ray K., Sadhna S., Pandey A.K., Sreelakshmi Y., Sharma R. Metabolomic homeostasis shifts after callus formation and shoot regeneration in tomato. PLoS ONE. 2017;12:e0176978. doi: 10.1371/journal.pone.0176978. PubMed DOI PMC

Xiong Y., McCormack M., Li L., Hall Q., Xiang C., Sheen J. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature. 2013;496:181–186. doi: 10.1038/nature12030. PubMed DOI PMC

Pfeiffer A., Janocha D., Dong Y., Medzihradszky A., Schöne S., Daum G., Suzaki T., Forner J., Langenecker T., Rempel E., et al. Intergation of light and metabolic signals for stem cell activation at the shoot apical meristem. eLife. 2016;5:e17023. doi: 10.7554/eLife.17023. PubMed DOI PMC

Ćosić T., Motyka V., Savić J., Raspor M., Marković M., Dobrev P.I., Ninković S. Sucrose interferes with endogenous cytokinin homeostasis and expression of organogenesis-related genes during de novo shoot organogenesis in kohlrabi. Sci. Rep. 2021;11:6494. doi: 10.1038/s41598-021-85932-w. PubMed DOI PMC

Lomin S.N., Myakushina Y.A., Arkhipov D.V., Leonova O.G., Popenko V.I., Schmülling T., Romanov G.A. Studies of cytokinin receptor-phosphotransmitter interaction provide evidences for the initiation of cytokinin signalling in the endoplasmic reticulum. Funct. Plant Biol. 2018;45:192–202. doi: 10.1071/FP16292. PubMed DOI

Romanov G.A., Lomin S.N., Schmülling T. Cytokinin signaling: From the ER or from the PM? That is the question! New Phytol. 2018;218:41–53. doi: 10.1111/nph.14991. PubMed DOI

Adamowski M., Friml J. PIN-dependent auxin transport: Action, regulation, and evolution. Plant Cell. 2015;27:20–32. doi: 10.1105/tpc.114.134874. PubMed DOI PMC

Singh G., Retzer K., Vosolsobě S., Napier R. Advances in understanding the mechanism of action of the auxin permease AUX1. Int. J. Mol. Sci. 2018;19:3391. doi: 10.3390/ijms19113391. PubMed DOI PMC

Zhou J.J., Luo J. The PIN-FORMED auxin efflux carriers in plants. Int. J. Mol. Sci. 2018;19:2759. doi: 10.3390/ijms19092759. PubMed DOI PMC

Ganguly A., Park M., Kesawat M.S., Cho H.T. Functional analysis of the hydrophilic loop in intracellular trafficking of arabidopsis PIN-FORMED proteins. Plant Cell. 2014;26:1570–1585. doi: 10.1105/tpc.113.118422. PubMed DOI PMC

Simon S., Skůpa P., Viaene T., Zwiewka M., Tejos R., Klíma P., Čarná M., Rolčík J., De Rycke R., Moreno I., et al. PIN6 auxin transporter at endoplasmic reticulum and plasma membrane mediates auxin homeostasis and organogenesis in arabidopsis. New Phytol. 2016;211:65–74. doi: 10.1111/nph.14019. PubMed DOI

Tanaka H., Dhonukshe P., Brewer P.B., Friml J. Spatiotemporal ASYMMETRIC auxin distribution: A means to coordinate plant development. Cell Mol. Life Sci. 2006;63:2738–2754. doi: 10.1007/s00018-006-6116-5. PubMed DOI PMC

Dhonukshe P., Aniento F., Hwang I., Robinson D.G., Mravec J., Stierhof Y.D., Friml J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in arabidopsis. Curr. Biol. 2007;17:520–527. doi: 10.1016/j.cub.2007.01.052. PubMed DOI

Zažímalová E., Murphy A.S., Yang H., Hoyerová K., Hošek P. Auxin transporters—Why so many? Cold Spring Harb. Perspect. Biol. 2010;2:a001552. doi: 10.1101/cshperspect.a001552. PubMed DOI PMC

Enders T.A., Strader L.C. Auxin activity: Past, present, and future. Am. J. Bot. 2015;102:180–196. doi: 10.3732/ajb.1400285. PubMed DOI PMC

Yang H., Murphy A.S. Functional expression and characterization of Arabidopsis ABCB, AUX1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J. 2009;59:179–191. doi: 10.1111/j.1365-313X.2009.03856.x. PubMed DOI

Petrášek J., Mravec J., Bouchard R., Blakeslee J.J., Abas M., Seifertová D., Wiśniewska J., Tadele Z., Kubeš M., Čovanová M., et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science. 2006;312:914–918. doi: 10.1126/science.1123542. PubMed DOI

Blakeslee J., Bandyopadhyay A., Lee O.R., Mravec J., Titapiwatanakun B., Sauer M., Makam S.N., Cheng Y., Bouchard R., Adamec J., et al. Interactions among PIN-FORMED and P-glycoprotein auxin transporters in arabidopsis. Plant Cell. 2007;19:131–147. doi: 10.1105/tpc.106.040782. PubMed DOI PMC

Barbosa I.C.R., Hammes U.Z., Schwehheimer C. Activation and polarity control of PIN-FORMED auxin transporters by phosphorylation. Trends Plant Sci. 2018;23:523–538. doi: 10.1016/j.tplants.2018.03.009. PubMed DOI

Tan S., Luschnig C., Friml J. Pho-view of auxin: Reversible Protein phosphorylation in auxin biosynthesis, transport and signaling. Mol. Plant. 2021;14:151–165. doi: 10.1016/j.molp.2020.11.004. PubMed DOI

Michniewicz M., Zago M.K., Abas L., Weijers D., Schweighofer A., Meskiene I., Heisler M.G., Ohno C., Zhang J., Huang F., et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell. 2007;130:1044–1056. doi: 10.1016/j.cell.2007.07.033. PubMed DOI

Guo X., Qin Q., Yan J., Niu Y., Huang B., Guan L., Li Y., Ren D., Li J., Hou S. TYPE-ONE PROTEIN PHOSPHATASE4 regulates pavement cell interdigitation by modulating PIN-FORMED1 polarity and trafficking in arabidopsis. Plant Physiol. 2015;167:1058–1075. doi: 10.1104/pp.114.249904. PubMed DOI PMC

Dai M., Zhang C., Kania U., Chen F., Xue Q., Mccray T., Li G., Qin G., Wakeley M., Terzaghi W., et al. A PP6-type phosphatase holoenzyme directly regulates PIN phosphorylation and auxin efflux in arabidopsis. Plant Cell. 2012;24:2497–2514. doi: 10.1105/tpc.112.098905. PubMed DOI PMC

Furutani M., Kajiwara T., Kato T., Treml B.S., Stockum C., Torres-Ruiz R.A., Tasaka M. The Gene MACCHI-BOU4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development. 2007;134:3849–3859. doi: 10.1242/dev.009654. PubMed DOI

Furutani M., Sakamoto N., Yoshida S., Kajiwara T., Robert H.S., Friml J., Tasaka M. Polar-Localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development. 2011;138:2069–2078. doi: 10.1242/dev.057745. PubMed DOI

Furutani M., Hirano Y., Nishimura T., Nakamura M., Taniguchi M., Suzuki K., Oshida R., Kondo C., Sun S., Kato K., et al. Polar recruitment of RLD by LAZY1-Like protein during gravity signaling in root branch angle control. Nat. Commun. 2020;11:76. doi: 10.1038/s41467-019-13729-7. PubMed DOI PMC

Garay-Arroyo A., Ortiz-Moreno E., de la Paz Sánchez M., Murphy A.S., García-Ponce B., Marsch-Martínez N., de Folter S., Corvera-Poiré A., Jaimes-Miranda F., Pacheco-Escobedo M.A., et al. The MADS transcription factor XAL2/AGL14 modulates auxin transport during arabidopsis root development by regulating PIN expression. EMBO J. 2013;32:2884–2895. doi: 10.1038/emboj.2013.216. PubMed DOI PMC

Cui D., Zhao J., Jing Y., Fan M., Liu J., Wang Z., Xin W., Hu Y. The Arabidopsis IDD14, IDD15, and IDD16 cooperatively regulate lateral organ morphogenesis and gravitropism by promoting auxin biosynthesis and transport. PLoS Genet. 2013;9:e1003759. doi: 10.1371/journal.pgen.1003759. PubMed DOI PMC

Bhatia N., Bozorg B., Larsson A., Ohno C., Jönsson H., Heisler M.G. Auxin acts through MONOPTEROS to regulate plant cell polarity and pattern phyllotaxis. Curr. Biol. 2016;26:3202–3208. doi: 10.1016/j.cub.2016.09.044. PubMed DOI PMC

Geisler M., Aryal B., di Donato M., Hao P. A critical view on ABC transporters and their interacting partners in auxin transport. Plant Cell Physiol. 2017;58:1601–1614. doi: 10.1093/pcp/pcx104. PubMed DOI

Santelia D., Vincenzetti V., Azzarello E., Bovet L., Fukao Y., Düchtig P., Mancuso S., Martinoia E., Geisler M. MDR-Like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Lett. 2005;579:5399–5406. doi: 10.1016/j.febslet.2005.08.061. PubMed DOI

Terasaka K., Blakeslee J.J., Titapiwatanakun B., Peer W.A., Bandyopadhyay A., Makam S.N., Lee O.R., Richards E.L., Murphy A.S., Sato F., et al. PGP4, an ATP-binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell. 2005;17:2922–2939. doi: 10.1105/tpc.105.035816. PubMed DOI PMC

Cho M., Lee S.H., Cho H.T. P-glycoprotein4 displays auxin efflux transporter-like action in arabidopsis root hair cells and tobacco cells. Plant Cell. 2007;19:3930–3943. doi: 10.1105/tpc.107.054288. PubMed DOI PMC

Kamimoto Y., Terasaka K., Hamamoto M., Takanashi K., Fukuda S., Shitan N., Sugiyama A., Suzuki H., Shibata D., Wang B., et al. Arabidopsis ABCB21 is a facultative auxin importer/exporter regulated by cytoplasmic auxin concentration. Plant Cell Physiol. 2012;53:2090–2100. doi: 10.1093/pcp/pcs149. PubMed DOI

Geisler M., Blakeslee J.J., Bouchard R., Lee O.R., Vincenzetti V., Bandyopadhyay A., Titapiwatanakun B., Peer W.A., Bailly A., Richards E.L., et al. Cellular efflux of auxin catalyzed by the arabidopsis MDR/PGP transporter AtPGP1. Plant J. 2005;44:179–194. doi: 10.1111/j.1365-313X.2005.02519.x. PubMed DOI

Lewis D.R., Miller N.D., Splitt B.L., Wu G., Spalding E.P. Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis Multidrug Resistance-Like ABC transporter genes. Plant Cell. 2007;19:1838–1850. doi: 10.1105/tpc.107.051599. PubMed DOI PMC

Henrichs S., Wang B., Fukao Y., Zhu J., Charrier L., Bailly A., Oehring S.C., Linnert M., Weiwad M., Endler A., et al. Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO J. 2012;31:2965–2980. doi: 10.1038/emboj.2012.120. PubMed DOI PMC

Pařízková B., Pernisová M., Novák O. What has been seen cannot be unseen—Detecting auxin in vivo. Int. J. Mol. Sci. 2017;18:2736. doi: 10.3390/ijms18122736. PubMed DOI PMC

Swarup R., Bhosale R. Developmental Roles of AUX1/LAX auxin influx carriers in plants. Front. Plant Sci. 2019;10:1306. doi: 10.3389/fpls.2019.01306. PubMed DOI PMC

Swarup K., Benková E., Swarup R., Casimiro I., Péret B., Yang Y., Parry G., Nielsen E., De Smet I., Vanneste S., et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 2008;10:946–954. doi: 10.1038/ncb1754. PubMed DOI

Yang Y., Hammes U.Z., Taylor C.G., Schachtman D.P., Nielsen E. High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 2006;16:1123–1127. doi: 10.1016/j.cub.2006.04.029. PubMed DOI

Strader L.C., Bartel B. Transport and metabolism of the endogenous auxin precursor indole-3-Butyric acid. Mol. Plant. 2011;4:477–486. doi: 10.1093/mp/ssr006. PubMed DOI PMC

Péret B., Swarup K., Ferguson A., Seth M., Yang Y., Dhondt S., James N., Casimiro I., Perry P., Syed A., et al. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during arabidopsis development. Plant Cell. 2012;24:2874–2885. doi: 10.1105/tpc.112.097766. PubMed DOI PMC

Krouk G., Lacombe B., Bielach A., Perrine-Walker F., Malinska K., Mounier E., Hoyerova K., Tillard P., Leon S., Ljung K., et al. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell. 2010;18:927–937. doi: 10.1016/j.devcel.2010.05.008. PubMed DOI

Wen Z., Kaiser B.N. Unraveling the functional role of NPF6 transporters. Front. Plant Sci. 2018;9:973. doi: 10.3389/fpls.2018.00973. PubMed DOI PMC

Asim M., Ullah Z., Xu F., An L., Aluko O.O., Wang Q., Liu H. Nitrate Signaling, functions, and regulation of root system architecture: Insights from Arabidopsis thaliana. Genes. 2020;11:633. doi: 10.3390/genes11060633. PubMed DOI PMC

Lay-Pruitt K.S., Takahashi H. Integrating N signals and root growth: The role of nitrate transceptor NRT1.1 in auxin-mediated lateral root development. J. Exp. Bot. 2020;71:4365–4368. doi: 10.1093/jxb/eraa243. PubMed DOI PMC

Wang W., Hu B., Li A., Chu C. NRT1.1s in plants: Functions beyond nitrate transport. J. Exp. Bot. 2020;71:4373–4379. doi: 10.1093/jxb/erz554. PubMed DOI PMC

Maghiaoui A., Bouguyon E., Cuesta C., Perrine-Walker F., Alcon C., Krouk G., Benková E., Nacry P., Gojon A., Bach L. The Arabidopsis NRT1.1 Transceptor coordinately controls auxin biosynthesis and transport to regulate root branching in response to nitrate. J. Exp. Bot. 2020;71:4480–4494. doi: 10.1093/jxb/eraa242. PubMed DOI

Barbez E., Kubeš M., Rolčík J., Béziat C., Pěnčík A., Wang B., Rosquete M.R., Zhu J., Dobrev P.I., Lee Y., et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature. 2012;485:119–122. doi: 10.1038/nature11001. PubMed DOI

Béziat C., Barbez E., Feraru M.I., Lucyshyn D., Kleine-Vehn J. Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition. Nat. Plants. 2017;3:17105. doi: 10.1038/nplants.2017.105. PubMed DOI PMC

Ranocha P., Dima O., Nagy R., Felten J., Corratgé-Faillie C., Novák O., Morreel K., Lacombe B., Martinez Y., Pfrunder S., et al. Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homeostasis. Nat. Commun. 2013;4:2625. doi: 10.1038/ncomms3625. PubMed DOI PMC

Skalický V., Kubeš M., Napier R., Novák O. Auxins and Cytokinins—The role of subcellular organization on homeostasis. Int. J. Mol. Sci. 2018;19:3115. doi: 10.3390/ijms19103115. PubMed DOI PMC

Herud-Sikimić O., Stiel A.C., Kolb M., Shanmugaratnam S., Berendzen K.W., Feldhaus C., Höcker B., Jürgens G. A biosensor for the direct visualization of auxin. Nature. 2021;592:768–772. doi: 10.1038/s41586-021-03425-2. PubMed DOI PMC

Bajguz A., Piotrowska A. Conjugates of auxin and cytokinin. Phytochemistry. 2009;70:957–969. doi: 10.1016/j.phytochem.2009.05.006. PubMed DOI

Eyer L., Vain T., Pařízková B., Oklestkova J., Barbez E., Kozubíková H., Pospíšil T., Wierzbicka R., Kleine-Vehn J., Fránek M., et al. 2,4-D and IAA amino acid conjugates show distinct metabolism in arabidopsis. PLoS ONE. 2016;11:e0159269. doi: 10.1371/journal.pone.0159269. PubMed DOI PMC

Auer C.A., Cohen J.D., Laloue M., Cooke T.J. Comparison of benzyl adenine metabolism in two Petunia hybrida lines differing in shoot organogenesis. Plant Physiol. 1992;98:1035–1041. doi: 10.1104/pp.98.3.1035. PubMed DOI PMC

Klemš M., Slámová Z., Motyka V., Malbeck J., Trávníčková A., Macháčková I., Holík J., Procházka S. Changes in cytokinin levels and metabolism in tobacco (Nicotiana tabacum L.) Explants during in vitro shoot organogenesis induced by trans-Zeatin and Dihydrozeatin. Plant Growth Regul. 2011;65:427–437. doi: 10.1007/s10725-011-9612-z. DOI

Montalbán I.A., Novák O., Rolčik J., Strnad M., Moncaleán P. Endogenous cytokinin and auxin profiles during in vitro organogenesis from vegetative buds of Pinus radiata adult trees. Physiol. Plant. 2013;148:214–231. doi: 10.1111/j.1399-3054.2012.01709.x. PubMed DOI

Aremu A.O., Plačková L., Bairu M.W., Novák O., Plíhalová L., Doležal K., Finnie J.F., Van Staden J. How does exogenously applied cytokinin type affect growth and endogenous cytokinins in micropropagated Merwilla plumbea? Plant Cell Tissue Organ Cult. 2014;118:245–256. doi: 10.1007/s11240-014-0477-5. DOI

Hallmark H.T., Černý M., Brzobohatý B., Rashotte A.M. Trans-Zeatin-N-Glucosides Have Biological Activity in Arabidopsis thaliana. PLoS ONE. 2020;15:e0232762. doi: 10.1371/journal.pone.0232762. PubMed DOI PMC

Hallmark H.T., Rashotte A.M. Cytokinin isopentenyladenine and its glucoside isopentenyladenine-9G delay leaf senescence through activation of cytokinin-associated genes. Plant Direct. 2020;4:e00292. doi: 10.1002/pld3.292. PubMed DOI PMC

Vylíčilová H., Bryksová M., Matušková V., Doležal K., Plíhalova L., Strnad M. Naturally Occurring and Artificial N9-Cytokinin Conjugates: From Synthesis to Biological Activity and Back. Biomolecules. 2020;10:832. doi: 10.3390/biom10060832. PubMed DOI PMC

Pokorná E., Hluska T., Galuszka P., Hallmark H.T., Dobrev P.I., Záveská Drábková L., Filipi T., Holubová K., Plíhal O., Rashotte A.M., et al. Cytokinin N-glucosides: Occurence, metabolism and biological activities in plants. Biomolecules. 2021;11:24. doi: 10.3390/biom11010024. PubMed DOI PMC

Hošek P., Hoyerová K., Kiran N.S., Dobrev P.I., Zahajská L., Filepová R., Motyka V., Müller K., Kamínek M. Distinct Metabolism of N-Glucosides of Isopentenyladenine and trans-Zeatin Determines Cytokinin Metabolic Spectrum in Arabidopsis. New Phytol. 2020;225:2423–2438. doi: 10.1111/nph.16310. PubMed DOI

Hoyerová K., Hošek P. New Insights into the Metabolism and Role of Cytokinin N-Glucosides in Plants. Front. Plant Sci. 2020;11:741. doi: 10.3389/fpls.2020.00741. PubMed DOI PMC

Durán-Medina Y., Díaz-Ramírez D., Marsch-Martínez N. Cytokinins on the move. Front. Plant Sci. 2017;8:146. doi: 10.3389/fpls.2017.00146. PubMed DOI PMC

Nedvĕd D., Hošek P., Klíma P., Hoyerová K. Differential subcellular distribution of cytokinins: How does membrane transport fit into the big picture? Int. J. Mol. Sci. 2021;22:3428. doi: 10.3390/ijms22073428. PubMed DOI PMC

Bürkle L., Cedzich A., Döpke C., Stransky H., Okumoto S., Gillissen B., Kühn C., Frommer W.B. Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of arabidopsis. Plant J. 2003;34:13–26. doi: 10.1046/j.1365-313X.2003.01700.x. PubMed DOI

Zürcher E., Liu J., di Donato M., Geisler M., Müller B. Plant development regulated by cytokinin sinks. Science. 2016;353:1027–1030. doi: 10.1126/science.aaf7254. PubMed DOI

Xiao Y., Liu D., Zhang G., Gao S., Liu L., Xu F., Che R., Wang Y., Tong H., Chu C. Big grain3, encoding a purine permease, regulates grain size via modulating cytokinin transport in rice. J. Integr. Plant Biol. 2019;61:581–597. doi: 10.1111/jipb.12727. PubMed DOI

Xiao Y., Zhang J., Yu G., Lu X., Mei W., Deng H., Zhang G., Chen G., Chu C., Tong H., et al. Endoplasmic reticulum-localized PURINE PERMEASE1 regulates plant height and grain weight by modulating cytokinin distribution in rice. Front. Plant Sci. 2020;11:618560. doi: 10.3389/fpls.2020.618560. PubMed DOI PMC

Mansfield T.A., Schultes N.P., Mourad G.S. AtAzg1 and AtAzg2 comprise a novel family of purine transporters in arabidopsis. FEBS Lett. 2009;583:481–486. doi: 10.1016/j.febslet.2008.12.048. PubMed DOI

Tessi T.M., Brumm S., Winklbauer E., Schumacher B., Pettinari G., Lescano I., González C.A., Wanke D., Maurino V.G., Harter K., et al. Arabidopsis AZG2 transports cytokinins in vivo and regulates lateral root emergence. New Phytol. 2021;229:979–993. doi: 10.1111/nph.16943. PubMed DOI

Tessi T.M., Shahriari M., Maurino V.G., Meissner E., Novak O., Pasternak T., Schumacher B.S., Flubacher N.S., Nautscher M., Williams A., et al. The auxin transporter PIN1 and the cytokinin transporter AZG1 interact to regulate the root stress response. bioRxiv. 2020;18:43. doi: 10.1101/2020.10.22.350363. DOI

Hirose N., Makita N., Yamaya T., Sakakibara H. Functional characterization and expression analysis of a gene, OsENT2, encoding an equilibrative nucleoside transporter in rice suggest a function in cytokinin transport. Plant Physiol. 2005;138:196–206. doi: 10.1104/pp.105.060137. PubMed DOI PMC

Sun J., Hirose N., Wang X., Wen P., Xue L., Sakakibara H., Zuo J. Arabidopsis SOI33/AtENT8 gene encodes a putative equilibrative nucleoside transporter that is involved in cytokinin transport in planta. J. Integr. Plant Biol. 2005;47:588–603. doi: 10.1111/j.1744-7909.2005.00104.x. DOI

Hirose N., Takei K., Kuroha T., Kamada-Nobusada T., Hayashi H., Sakakibara H. Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot. 2008;59:75–83. doi: 10.1093/jxb/erm157. PubMed DOI

Bishopp A., Lehesranta S., Vatén A., Help H., El-Showk S., Scheres B., Helariutta K., Mähönen A.P., Sakakibara H., Helariutta Y. Phloem-Transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr. Biol. 2011;21:927–932. doi: 10.1016/j.cub.2011.04.049. PubMed DOI

Ko D., Kang J., Kiba T., Park J., Kojima M., Do J., Kim K.Y., Kwon M., Endler A., Song W.Y., et al. Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc. Natl. Acad. Sci. USA. 2014;111:7150–7155. doi: 10.1073/pnas.1321519111. PubMed DOI PMC

Zhang K., Novak O., Wei Z., Gou M., Zhang X., Yu Y., Yang H., Cai Y., Strnad M., Liu C.J. Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat. Commun. 2014;5:3274. doi: 10.1038/ncomms4274. PubMed DOI

Jiskrová E., Novák O., Pospíšilová H., Holubová K., Karády M., Galuszka P., Robert S., Frébort I. Extra- and intracellular distribution of cytokinins in the leaves of monocots and dicots. New Biotechnol. 2016;33:735–742. doi: 10.1016/j.nbt.2015.12.010. PubMed DOI

Osugi A., Kojima M., Takebayashi Y., Ueda N., Kiba T., Sakakibara H. Systemic transport of trans-zeatin and its precursor have differing roles in arabidopsis shoots. Nat. Plants. 2017;3:17112. doi: 10.1038/nplants.2017.112. PubMed DOI

Kudoyarova G.R., Korobova A.V., Akhiyarova G.R., Arkhipova T.N., Zaytsev D.Y., Prinsen E., Egutkin N.L., Medvedev S.S., Veselov S.Y. Accumulation of cytokinins in roots and their export to the shoots of durum wheat plants treated with the protonophore carbonyl cyanide m-chlorophenylhydrazone (CCCP) J. Exp. Bot. 2014;65:2287–2294. doi: 10.1093/jxb/eru113. PubMed DOI PMC

Romanov G.A., Schmülling T. Opening doors for cytokinin trafficking at the er membrane. Trends Plant Sci. 2021;26:305–308. doi: 10.1016/j.tplants.2021.02.006. PubMed DOI

Hluska T., Hlusková L., Emery R.J.N. The hulks and the deadpools of the cytokinin universe: A dual strategy for cytokinin production, translocation and signal transduction. Biomolecules. 2021;11:209. doi: 10.3390/biom11020209. PubMed DOI PMC

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