Abstract
De novo shoot organogenesis (DNSO) is a widely used procedure for obtaining regenerated plant shoots for biotechnological, industrial and conservation purposes. Particular morphogenic events leading to shoot regeneration are induced by plant hormones auxin and cytokinin that are exogenously supplemented to the regenerating explants through the nutrient media. It was shown, in Arabidopsis and in other plant species, that the early stages of DNSO are crucially dependent on auxin signaling and include the development of pluripotent primordia that are developmentally identical to lateral root primordia, whereas in the later stages, these primordia acquire the shoot identity and develop a shoot apical meristem (SAM) in a process that is governed mostly by cytokinin, but is also influenced by auxin signaling. In this chapter, we discuss the current state of knowledge about the particular components of auxin and cytokinin signaling that are specifically involved in the phytohormonal regulation of DNSO. Throughout DNSO, the auxin signaling multicellular domains are generated through the action of auxin influx and efflux carriers, whereas AUXIN RESPONSE FACTORs (ARFs), that are modulated by the Aux/IAA repressors, regulate gene expression during various stages of DNSO. Conversely, the cytokinin signals relevant for DNSO are perceived overwhelmingly through the receptor ARABIDOPSIS HISTIDINE KINASE4 (AHK4) and effected through the type-B ARABIDOPSIS RESPONSE REGULATORs (ARRs), whereas type-A ARRs act as attenuators of the cytokinin signals. Throughout DNSO, auxin and cytokinin signals enter mutual crosstalk, and crosstalk with other phytohormones, sugars and other developmental signals, for a complex and fine-tuned regulation of shoot regeneration.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Adamowski M, Friml J (2015) PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27:20–32. https://doi.org/10.1105/tpc.114.134874
Adibi M, Yoshida S, Weijers D, Fleck C (2016) Centering the organizing center in the Arabidopsis thaliana shoot apical meristem by a combination of cytokinin signaling and self-organization. PLoS ONE 11:e0147830. https://doi.org/10.1371/journal.pone.0147830
Alvarez JM, Bueno N, Cuesta C, Feito I, Ordás RJ (2020) Hormonal and gene dynamics in de novo shoot meristem formation during adventitious caulogenesis in cotyledons of Pinus pinea. Plant Cell Rep 39:527–541. https://doi.org/10.1007/s00299-020-02508-0
Antoniadi I, Novák O, Gelová Z, Johnson A, Plíhal O, Simerský R, Mik V, Vain T, Mateo-Bonmatí E, Karady M, Pernisová M, Plačková L, Opassathian K, Hejátko J, Robert S, Friml J, Doležal K, Ljung K, Turnbull C (2020) Cell-surface receptors enable perception of extracellular cytokinins. Nat Commun 11:4284. https://doi.org/10.1038/s41467-020-17700-9
Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, Etheridge N, Argyros DA, Mason MG, Kieber JJ, Schaller GE (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20:2102–2116. https://doi.org/10.1105/tpc.108.059584
Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc’h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57:626–644. https://doi.org/10.1111/j.1365-313X.2008.03715.x
Banno H, Ikeda Y, Niu QW, Chua NH (2001) Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618. https://doi.org/10.1105/tpc.010234
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602. https://doi.org/10.1016/S0092-8674(03)00924-3
Berckmans B, Vassileva V, Schmid SPC, Maes S, Parizot B, Naramoto S, Magyar Z, Kamei CLA, Koncz C, Bögre L, Persiau G, De Jaeger G, Friml J, Simon R, Beeckman T, De Veylder L (2011) Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by LATERAL ORGAN BOUNDARY proteins. Plant Cell 23:3671–3683. https://doi.org/10.1105/tpc.111.088377
Buechel S, Leibfried A, To JPC, Zhao Z, Andersen SU, Kieber JJ, Lohmann JU (2010) Role of A-type ARABIDOPSIS RESPONSE REGULATORS in meristem maintenance and regeneration. Eur J Cell Biol 89:279–284. https://doi.org/10.1016/j.ejcb.2009.11.016
Cary AJ, Che P, Howell SH (2002) Developmental events and shoot apical meristem gene expression patterns during shoot development in Arabidopsis thaliana. Plant J 32:867–877. https://doi.org/10.1046/j.1365-313X.2002.01479.x
Chang L, Ramireddy E, Schmülling T (2013) Lateral root formation and growth of Arabidopsis is redundantly regulated by cytokinin metabolism and signalling genes. J Exp Bot 64:5021–5032. https://doi.org/10.1093/jxb/ert291
Che P, Gingerich DJ, Lall S, Howell SH (2002) Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell 14:2771–2785. https://doi.org/10.1105/tpc.006668
Che P, Lall S, Howell SH (2007) Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture. Planta 226:1183–1194. https://doi.org/10.1007/s00425-007-0565-4
Che P, Lall S, Howell SH (2008) Acquiring competence for shoot development in Arabidopsis: ARR2 directly targets A-type ARR genes that are differentially activated by CIM preincubation. Plant Signal Behav 3:99–101. https://doi.org/10.4161/psb.3.2.4958
Cheng ZJ, Wang L, Sun W, Zhang Y, Zhou C, Su YH, Li W, Sun TT, Zhao XY, Li XG, Cheng Y, Zhao Y, **e Q, Zhang XS (2013) 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. https://doi.org/10.1104/pp.112.203166
Cheon J, Park SY, Schulz B, Choe S (2010) Arabidopsis brassinosteroid biosynthetic mutant dwarf7-1 exhibits slower rates of cell division and shoot induction. BMC Plant Biol 10:270. https://doi.org/10.1186/1471-2229-10-270
Chickarmane VS, Gordon SP, Tarr PT, Heisler MG, Meyerowitz EM (2012) Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc Natl Acad Sci USA 109:4002–4007. https://doi.org/10.1073/pnas.1200636109
Chung Y, Zhu Y, Wu MF, Simonini S, Kuhn A, Armenta-Medina A, ** R, Østergaard L, Gillmor CS, Wagner D (2019) Auxin response factors promote organogenesis by chromatin-mediated repression of the pluripotency gene SHOOTMERISTEMLESS. Nat Commun 10:886. https://doi.org/10.1038/s41467-019-08861-3
Ckurshumova W, Berleth T (2015) Overcoming recalcitrance—auxin response factor functions in plant regeneration. Plant Signal Behav 10:e993293. https://doi.org/10.4161/15592324.2014.993293
Ckurshumova W, Smirnova T, Marcos D, Zayed Y, Berleth T (2014) Irrepressible MONOPTEROS/ARF5 promotes de novo shoot formation. New Phytol 204:556–566. https://doi.org/10.1111/nph.13014
Cortleven A, Marg I, Yamburenko MV, Schlicke H, Hill K, Grimm B, Schaller GE, Schmülling T (2016) Cytokinin regulates the etioplast-chloroplast transition through the two-component signaling system and activation of chloroplast-related genes. Plant Physiol 172:464–478. https://doi.org/10.1104/pp.16.00640
Ćosić T, Motyka V, Raspor M, Savić J, Cingel A, Vinterhalter B, Vinterhalter D, Trávníčková A, Dobrev PI, Bohanec B, Ninković S (2015) 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 Tiss Organ Cult 121:741–760. https://doi.org/10.1007/s11240-015-0742-2
Ćosić T, Raspor M, Savić J, Cingel A, Matekalo D, Zdravković-Korać S, Ninković S (2019) 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 232:257–269. https://doi.org/10.1016/j.jplph.2018.11.004
Ćosić T, Savić J, Raspor M, Cingel A, Ghalawnji N, Vinterhalter B, Ninković S (2020) Effects of different types of sugars and plant growth regulators on kohlrabi seedling growth and development in vitro. Arch Biol Sci 72:349–357. https://doi.org/10.2298/ABS200622029C
Ćosić T, Motyka V, Savić J, Raspor M, Marković M, Dobrev PI, Ninković S (2021) Sucrose interferes with endogenous cytokinin homeostasis and expression of organogenesis-related genes during de novo shoot organogenesis in kohlrabi. Sci Rep 11:6494. https://doi.org/10.1038/s41598-021-85932-w
Dai X, Liu Z, Qiao M, Li J, Li S, **ang F (2017) ARR12 promotes de novo shoot regeneration in Arabidopsis thaliana via activation of WUSCHEL expression. J Integr Plant Biol 59:747–758. https://doi.org/10.1111/jipb.12567
Daimon Y, Takabe K, Tasaka M (2003) The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant Cell Physiol 44:113–121. https://doi.org/10.1093/pcp/pcg038
Das A, Sarkar S, Bhattacharyya S, Gantait S (2020) Biotechnological advancements in Catharanthus roseus (L.) G. Don. Appl Microbiol Biotechnol 104:4811–4835. https://doi.org/10.1007/s00253-020-10592-1
Das PK, Shin DH, Choi SB, Yoo SD, Choi G, Park YI (2012) Cytokinins enhance sugar-induced anthocyanin biosynthesis in Arabidopsis. Mol Cells 34:93–101. https://doi.org/10.1007/s10059-012-0114-2
De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S, Möller B, Wilson M, Holman T, Van Isterdael G, Brunoud G, Vuylsteke M, Vernoux T, De Veylder L, Inzé D, Weijers D, Bennett MJ, Beeckman T (2010) A novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol 20:1697–1706. https://doi.org/10.1016/j.cub.2010.09.007
De Smet I, Lau S, Voβ U, Vanneste S, Benjamins R, Rademacher EH, Schlereth A, De Rybel B, Vassileva V, Grunewald W, Naudts M, Levesque MP, Ehrismann JS, Inzé D, Luschnig C, Benfey PN, Weijers D, Van Montagu MCE, Bennett MJ, Jürgens G, Beeckman T (2010) Bimodular auxin response controls organogenesis in Arabidopsis. Proc Natl Acad Sci USA 107:2705–2710. https://doi.org/10.1073/pnas.0915001107
Efroni I, Mello A, Nawy T, Ip PL, Rahni R, DelRose N, Powers A, Satija R, Birnbaum KD (2016) Root regeneration triggers an embryo-like sequence guided by hormonal interactions. Cell 165:1721–1733. https://doi.org/10.1016/j.cell.2016.04.046
Fan M, Xu C, Xu K, Hu Y (2012) LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res 22:1169–1180. https://doi.org/10.1038/cr.2012.63
Farcot E, Lavedrine C, Vernoux T (2015) A modular analysis of the auxin signalling network. PLoS ONE 10:e0122231. https://doi.org/10.1371/journal.pone.0122231
Fehér A (2019) Callus, dedifferentiation, totipotency, somatic embryogenesis: what these terms mean in the era of molecular plant biology? Front Plant Sci 10:536. https://doi.org/10.3389/fpls.2019.00536
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. Plant J 29:153–168. https://doi.org/10.1046/j.0960-7412.2001.01201.x
Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J 44:382–395. https://doi.org/10.1111/j.1365-313X.2005.02537.x
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. https://doi.org/10.1111/j.1365-313X.2006.02882.x
García-Gómez ML, Azpeitia E, Álvarez-Buylla ER (2017) A dynamic gene-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana. PLoS Comput Biol 13:e1005488. https://doi.org/10.1371/journal.pcbi.1005488
Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H (2012) Multiple AUX-IAA/ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Phil Trans R Soc B 367:1461–1468. https://doi.org/10.1098/rstb.2011.0232
Gómez-Felipe A, Kierzkowski D, de Folter S (2021) The relationship between AGAMOUS and cytokinin signaling in the establishment of carpeloid features. Plants 10:827. https://doi.org/10.3390/plants10050827
Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134:3539–3548. https://doi.org/10.1242/dev.010298
Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci USA 106:16529–16534. https://doi.org/10.1073/pnas.0908122106
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460. https://doi.org/10.1016/j.pbi.2007.08.014
Higuchi M, Pischke MS, Mähönen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101:8821–8826. https://doi.org/10.1073/pnas.0402887101
Hisano H, Matsuura T, Mori IC, Yamane M, Sato K (2016) Endogenous hormone levels affect the regeneration ability of callus derived from different organs in barley. Plant Physiol Biochem 99:66–72. https://doi.org/10.1016/j.plaphy.2015.12.005
Hong L, Ye C, Lin J, Fu H, Wu X, Li QQ (2018) Alternative polyadenylation is involved in auxin-based plant growth and development. Plant J 93:246–258. https://doi.org/10.1111/tpj.13771
Horstman A, Willemsen V, Boutilier K, Heidstra R (2014) AINTEGUMENTA-LIKE proteins: hubs in a plethora of networks. Trends Plant Sci 19:146–157. https://doi.org/10.1016/j.tplants.2013.10.010
Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173. https://doi.org/10.1105/tpc.113.116053
Ikeuchi M, Iwase A, Rymen B, Lambolez A, Kojima M, Takebayashi Y, Heyman J, Watanabe S, Seo M, De Veylder L, Sakakibara H, Sugimoto K (2017) Wounding triggers callus formation via dynamic hormonal and transcriptional changes. Plant Physiol 175:1158–1174. https://doi.org/10.1104/pp.17.01035
Ikeuchi M, Shibata M, Rymen B, Iwase A, Bågman AM, Watt L, Coleman D, Favero DS, Takahashi T, Ahnert SE, Brady SM, Sugimoto K (2018) A gene regulatory network for cellular reprogramming in plant regeneration. Plant Cell Physiol 59:770–782. https://doi.org/10.1093/pcp/pcy013
Ikeuchi M, Favero DS, Sakamoto Y, Iwase A, Coleman D, Rymen B, Sugimoto K (2019) Molecular mechanisms of plant regeneration. Annu Rev Plant Biol 70:377–406. https://doi.org/10.1146/annurev-arplant-050718-100434
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. https://doi.org/10.1093/pcp/pcm165
Iwase A, Mitsuda N, Koyama T, Hiratsu K, Kojima M, Arai T, Inoue Y, Seki M, Sakakibara H, Sugimoto K, Ohme-Takagi M (2011) The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21:508–514. https://doi.org/10.1016/j.cub.2011.02.020
Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565. https://doi.org/10.1016/j.cub.2005.07.023
Kakani A, Li G, Peng Z (2009) 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 229:645–657. https://doi.org/10.1007/s00425-008-0846-6
Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev PV, Pinon V, Meyerowitz EM, Scheres B, Prasad K (2015) PLETHORA genes control regeneration by a two-step mechanism. Curr Biol 25:1017–1030. https://doi.org/10.1016/j.cub.2015.02.022
Kareem A, Radhakrishnan D, Wang X, Bagavathiappan S, Trivedi ZB, Sugimoto K, Xu J, Mähönen AP, Prasad K (2016) Protocol: a method to study the direct reprogramming of lateral primordia to fertile shoots. Plant Methods 12:27. https://doi.org/10.1186/s13007-016-0127-5
Kaur A, Reddy MS, Kumar A (2017) Efficient, one step and cultivar independent shoot organogenesis of potato. Physiol Mol Biol Plants 23:461–469. https://doi.org/10.1007/s12298-017-0418-y
Kieber JJ, Schaller GE (2018) Cytokinin signaling in plant development. Development 145:dev149344. https://doi.org/10.1242/dev.149344
Kim JY, Yang W, Forner J, Lohmann JU, Noh B, Noh YS (2018) Epigenetic reprogramming by histone acetyltransferase HAG1/AtGCN5 is required for pluripotency acquisition in Arabidopsis. EMBO J 37:e98726. https://doi.org/10.15252/embj.201798726
Kim SH, Bahk S, An J, Hussain S, Nguyen NT, Do HL, Kim JY, Hong JC, Chung WS (2020) A gain-of-function mutant of IAA15 inhibits lateral root development by transcriptional repression of LBD genes in Arabidopsis. Front Plant Sci 11:1239. https://doi.org/10.3389/fpls.2020.01239
Kim SL, Lee Y, Lee SH, Kim SH, Han TJ, Kim SK (2008) Brassinolide influences the regeneration of adventitious shoots from cultured leaf discs of tobacco. J Plant Biol 51:221–226. https://doi.org/10.1007/BF03030702
Koike I, Taniguchi K, Shimomura K, Umehara M (2017) Dynamics of endogenous indole-3-acetic acid and cytokinins during adventitious shoot formation in ipecac. J Plant Growth Regul 36:805–813. https://doi.org/10.1007/s00344-017-9684-8
Kong D, Hao Y, Cui H (2016) The WUSCHEL RELATED HOMEOBOX protein WOX7 regulates the sugar response of lateral root development in Arabidopsis thaliana. Mol Plant 9:261–270. https://doi.org/10.1016/j.molp.2015.11.006
Krogan NT, Ckurshumova W, Marcos D, Caragea AE, Berleth T (2012) Deletion of MP/ARF5 domains III and IV reveals a requirement for Aux/IAA regulation in Arabidopsis leaf vascular patterning. New Phytol 194:391–401. https://doi.org/10.1111/j.1469-8137.2012.04064.x
Krogan NT, Marcos D, Weiner AI, Berleth T (2016) 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 212:42–50. https://doi.org/10.1111/nph.14107
Laskowski M, Grieneisen VA, Hofhuis H, ten Hove CA, Hogeweg P, Marée AFM, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6:e307. https://doi.org/10.1371/journal.pbio.0060307
Lau S, De Smet I, Kolb M, Meinhardt H, Jürgens G (2011) Auxin triggers a genetic switch. Nat Cell Biol 13:611–615. https://doi.org/10.1038/ncb2212
Lee HW, Kim NY, Lee DJ, 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. https://doi.org/10.1104/pp.109.143685
Lee K, Seo PJ (2017) Arabidopsis TOR signaling is essential for sugar-regulated callus formation. J Integr Plant Biol 59:742–746. https://doi.org/10.1111/jipb.12560
Lee MH, Lee J, Jie EY, Choi SH, Jiang L, Ahn WS, Kim CY, Kim SW (2020) 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 21:5309. https://doi.org/10.3390/ijms21155309
Leibfried A, To JPC, Busch W, Stehling S, Kehle A, Demar M, Kieber JJ, Lohmann JU (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438:1172–1175. https://doi.org/10.1038/nature04270
Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7:e1002243. https://doi.org/10.1371/journal.pgen.1002243
Liu J, Hu X, Qin P, Prasad K, Hu Y, Xu L (2018) The WOX11-LBD16 pathway promotes pluripotency acquisition in callus cells during de novo shoot regeneration in tissue culture. Plant Cell Physiol 59:739–748. https://doi.org/10.1093/pcp/pcy010
Liu Z, Dai X, Li J, Liu N, Liu X, Li S, **ang F (2020) The type-B cytokinin response regulator ARR1 inhibits shoot regeneration in an ARR12-dependent manner in Arabidopsis. Plant Cell 32:2271–2291. https://doi.org/10.1105/tpc.19.00022
Lombardi-Crestana S, da Silva Azevedo M, Ferreira e Silva GF, Pino LE, Appezzato-da-Glória B, Figueira A, Nogueira FTS, Peres LEP (2012) The tomato (Solanum lycopersicum cv Micro-Tom) natural genetic variation Rg1 and the DELLA mutant procera control the competence necessary to form adventitious roots and shoots. J Exp Bot 63:5689–5703. https://doi.org/10.1093/jxb/ers221
Lomin SN, Myakushina YA, Kolachevskaya OO, Getman IA, Arkhipov DV, Savelieva EM, Osolodkin DI, Romanov GA (2018) Cytokinin perception in potato: new features of canonical players. J Exp Bot 69:3839–3853. https://doi.org/10.1093/jxb/ery199
Lomin SN, Savelieva EM, Arkhipov DV, Pashkovskiy PP, Myakushina YA, Heyl A, Romanov GA (2021) Cytokinin perception in ancient plants beyond Angiospermae. Int J Mol Sci 22:13077. https://doi.org/10.3390/ijms222313077
Luo L, Zeng J, Wu H, Tian Z, Zhao Z (2018) A molecular framework for auxin-controlled homeostasis of shoot stem cells in Arabidopsis. Mol Plant 11:899–913. https://doi.org/10.1016/j.molp.2018.04.006
Ma Y, Miotk A, Šutiković Z, Ermakova O, Wenzl C, Medzihradszky A, Gaillochet C, Forner J, Utan G, Brackmann K, Galván-Ampudia CS, Vernoux T, Greb T, Lohmann JU (2019) WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis. Nat Commun 10:5093. https://doi.org/10.1038/s41467-019-13074-9
Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–597. https://doi.org/10.1105/tpc.010354
Marhavý P, Vanstraelen M, De Rybel B, Zhaojun D, Bennett MJ, Beeckman T, Benková E (2013) Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 32:149–158. https://doi.org/10.1038/emboj.2012.303
Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso JM, Ecker JR, Schaller GE (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17:3007–3018. https://doi.org/10.1105/tpc.105.035451
Meng WJ, Cheng ZJ, Sang YL, Zhang MM, Rong XF, Wang ZW, Tang YY, Zhang XS (2017) Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell 29:1357–1372. https://doi.org/10.1105/tpc.16.00640
Motte H, Vereecke D, Geelen D, Werbrouck S (2014) The molecular path to in vitro shoot regeneration. Biotechnol Adv 32:107–121. https://doi.org/10.1016/j.biotechadv.2013.12.002
Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 20:1138–1143. https://doi.org/10.1016/j.cub.2010.05.035
Muñoz A, Mangano S, González-García MP, Contreras R, Sauer M, De Rybel B, Weijers D, Sánchez-Serrano JJ, Sanmartín M, Rojo E (2017) RIMA-dependent nuclear accumulation of IYO triggers auxin-irreversible cell differentiation in Arabidopsis. Plant Cell 29:575–588. https://doi.org/10.1105/tpc.16.00791
Muro-Pastor MI, Gonzalez R, Strauss J, Narendja F, Scazzocchio C (1999) The GATA factor AreA is essential for chromatin remodelling in a eukaryotic bidirectional promoter. EMBO J 18:1584–1597. https://doi.org/10.1093/emboj/18.6.1584
Nedvěd D, Hošek P, Klíma P, Hoyerová K (2021) Differential subcellular distribution of cytokinins: how does membrane transport fit into the big picture? Int J Mol Sci 22:3428. https://doi.org/10.3390/ijms22073428
Neelakandan AK, Wang K (2012) Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications. Plant Cell Rep 31:597–620. https://doi.org/10.1007/s00299-011-1202-z
Nguyen KH, Ha CV, Nishiyama R, Watanabe Y, Leyva-González MA, Fujita Y, Tran UT, Li W, Tanaka M, Seki M, Schaller GE, Herrera-Estrella L, Tran LSP (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc Natl Acad Sci USA 113:3090–3095. https://doi.org/10.1073/pnas.1600399113
Niazian M, Noori SAS, Galuszka P, Tohidfar M, Mortazavian SMM (2017) Genetic stability of regenerated plants via indirect somatic embryogenesis and indirect shoot regeneration of Carum copticum L. Ind Crop Prod 97:330–337. https://doi.org/10.1016/j.indcrop.2016.12.044
Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlap** functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377. https://doi.org/10.1105/tpc.021477
Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlap** functions of ARF7 and ARF19. Plant Cell 17:444–463. https://doi.org/10.1105/tpc.104.028316
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. https://doi.org/10.1105/tpc.106.047761
Pasternak T, Lystvan K, Betekhtin A, Hasterok R (2020) From single cell to plants: mesophyll protoplasts as a versatile system for investigating plant cell reprogramming. Int J Mol Sci 21:4195. https://doi.org/10.3390/ijms21124195
Pernisova M, Grochova M, Konecny T, Plackova L, Harustiakova D, Kakimoto T, Heisler MG, Novak O, Hejatko J (2018) Cytokinin signalling regulates organ identity via the AHK4 receptor in Arabidopsis. Development 145:dev163907. https://doi.org/10.1242/dev.163907
Peterson MA, McMaster SA, Riechers DE, Skelton J, Stahlman PW (2016) 2,4-D: past, present, and future: a review. Weed Technol 30:303–345. https://doi.org/10.1614/WT-D-15-00131.1
Pfeiffer A, Janocha D, Dong Y, Medzihradszky A, Schöne S, Daum G, Suzaki T, Forner J, Langenecker T, Rempel E, Schmid M, Wirtz M, Hell R, Lohmann JU (2016) Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. eLife 5:e17023. https://doi.org/10.7554/eLife.17023.001
Piya S, Shrestha SK, Binder B, Stewart CN Jr, Hewezi T (2014) Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Front Plant Sci 5:744. https://doi.org/10.3389/fpls.2014.00744
Raspor M, Motyka V, Ninković S, Dobrev PI, Malbeck J, Ćosić T, Cingel A, Savić J, Tadić V, Dragićević IČ (2020) Endogenous levels of cytokinins, indole-3-acetic acid and abscisic acid in in vitro grown potato: a contribution to potato hormonomics. Sci Rep 10:3437. https://doi.org/10.1038/s41598-020-60412-9
Raspor M, Motyka V, Kaleri AR, Ninković S, Lj T, Cingel A, Ćosić T (2021) Integrating the roles for cytokinin and auxin in de novo shoot organogenesis: from hormone uptake to signaling outputs. Int J Mol Sci 22:8554. https://doi.org/10.3390/ijms22168554
Ren B, Liang Y, Deng Y, Chen Q, Zhang J, Yang X, Zuo J (2009) Genome-wide comparative analysis of type-A ARABIDOPSIS RESPONSE REGULATOR genes by overexpression studies reveals their diverse roles and regulatory mechanisms in cytokinin signaling. Cell Res 19:1178–1190. https://doi.org/10.1038/cr.2009.88
Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54. https://doi.org/10.1105/tpc.105.037796
Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13:465–480. https://doi.org/10.1105/tpc.13.3.465
Romanov GA, Schmülling T (2021) Opening doors for cytokinin trafficking at the ER membrane. Trends Plant Sci 26:305–308. https://doi.org/10.1016/j.tplants.2021.02.006
Romanov GA, Lomin SN, Schmülling T (2006) Biochemical characteristics and ligand-binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/AHK4 as revealed by a direct binding assay. J Exp Bot 57:4051–4058. https://doi.org/10.1093/jxb/erl179
Romanov GA, Lomin SN, Schmülling T (2018) Cytokinin signaling: from the ER or from the PM? That is the question! New Phytol 218:41–53. https://doi.org/10.1111/nph.14991
Roosjen M, Paque S, Weijers D (2018) Auxin response factors: output control in auxin biology. J Exp Bot 69:179–188. https://doi.org/10.1093/jxb/erx237
Rosspopoff O, Chelysheva L, Saffar J, Lecorgne L, Gey D, Caillieux E, Colot V, Roudier F, Hilson P, Berthomé R, Da Costa M, Rech P (2017) Direct conversion of root primordium into shoot meristem relies on timing of stem cell niche development. Development 144:1187–1200. https://doi.org/10.1242/dev.142570
Sakr S, Wang M, Dédaldéchamp F, Perez-Garcia MD, Ogé L, Hamama L, Atanassova R (2018) The sugar-signaling hub: overview of regulators and interaction with the hormonal and metabolic network. Int J Mol Sci 19:2506. https://doi.org/10.3390/ijms19092506
Santuari L, Sanchez-Perez GF, Luijten M, Rutjens B, Terpstra I, Berke L, Gorte M, Prasad K, Bao D, Timmermans-Hereijgers JLPM, Maeo K, Nakamura K, Shimotohno A, Pencik A, Novak O, Ljung K, van Heesch S, de Bruijn E, Cuppen E, Willemsen V, Mähönen AP, Lukowitz W, Snel B, de Ridder D, Scheres B, Heidstra R (2016) The PLETHORA gene regulatory network guides growth and cell differentiation in Arabidopsis roots. Plant Cell 28:2937–2951. https://doi.org/10.1105/tpc.16.00656
Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814. https://doi.org/10.1038/nature05703
Schaller GE, Bishopp A, Kieber JJ (2015) The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27:44–63. https://doi.org/10.1105/tpc.114.133595
Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11:118–130. https://pubmed.ncbi.nlm.nih.gov/13486467/
Stanišić M, Raspor M, Ninković S, Milošević S, Ćalić D, Bohanec B, Trifunović M, Petrić M, Subotić A, Jevremović S (2015) Clonal fidelity of Iris sibirica plants regenerated by somatic embryogenesis and organogenesis in leaf-base culture—RAPD and flow cytometer analyses. S Afr J Bot 96:42–52. https://doi.org/10.1016/j.sajb.2014.10.014
Stolz A, Riefler M, Lomin SN, Achazi K, Romanov GA, Schmülling T (2011) The specificity of cytokinin signalling in Arabidopsis thaliana is mediated by differing ligand affinities and expression profiles of the receptors. Plant J 67:157–168. https://doi.org/10.1111/j.1365-313X.2011.04584.x
Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471. https://doi.org/10.1016/j.devcel.2010.02.004
Taniguchi M, Sasaki N, Tsuge T, Aoyama T, Oka A (2007) ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant Cell Physiol 48:263–277. https://doi.org/10.1093/pcp/pcl063
Thakur J, Dwivedi MD, Sourabh P, Uniyal PL, Pandey AK (2016) Genetic homogeneity revealed using SCoT, ISSR and RAPD markers in micropropagated Pittosporum eriocarpum Royle—an endemic and endangered medicinal plant. PLoS ONE 11:e0159050. https://doi.org/10.1371/journal.pone.0159050
Tikendra L, Koijam AS, Nongdam P (2019) Molecular markers based genetic fidelity assessment of micropropagated Dendrobium chrysotoxum Lindl. Meta Gene 20:100562. https://doi.org/10.1016/j.mgene.2019.100562
To JPC, Haberer G, Ferreira FJ, Deruère J, Mason MG, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16:658–671. https://doi.org/10.1105/tpc.018978
Valvekens D, Van Montagu M, Van Lijsebettens M (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci USA 85:5536–5540. https://doi.org/10.1073/pnas.85.15.5536
Vangheluwe N, Beeckman T (2021) Lateral root initiation and the analysis of gene function using genome editing with CRISPR in Arabidopsis. Genes 12:884. https://doi.org/10.3390/genes12060884
Wang M, Le Gourrierec J, Jiao F, Demotes-Mainard S, Perez-Garcia MD, Ogé L, Hamama L, Crespel L, Bertheloot J, Chen J, Grappin P, Sakr S (2021) Convergence and divergence of sugar and cytokinin signaling in plant development. Int J Mol Sci 22:1282. https://doi.org/10.3390/ijms22031282
Weijers D, Benkova E, Jäger KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jürgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24:1874–1885. https://doi.org/10.1038/sj.emboj.7600659
Wulfetange K, Lomin SN, Romanov GA, Stolz A, Heyl A, Schmülling T (2011) The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol 156:1808–1818. https://doi.org/10.1104/pp.111.180539
Xu L (2018) De novo root regeneration from leaf explants: wounding, auxin, and cell fate transition. Curr Opin Plant Biol 41:39–45. https://doi.org/10.1016/j.pbi.2017.08.004
Yan Z, Wang J, Wang F, **e C, Lv B, Yu Z, Dai S, Liu X, **a G, Tian H, Li C, Ding Z (2021) MPK3/6-induced degradation of ARR1/10/12 promotes salt tolerance in Arabidopsis. EMBO Rep 22:e52457. https://doi.org/10.15252/embr.202152457
Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15:1566–1571. https://doi.org/10.1016/j.cub.2005.07.060
Yokoyama A, Yamashino T, Amano YI, Tajima Y, Imamura A, Sakakibara H, Mizuno T (2007) Type-B ARR transcription factors, ARR10 and ARR12, are implicated in cytokinin-mediated regulation of protoxylem differentiation in roots of Arabidopsis thaliana. Plant Cell Physiol 48:84–96. https://doi.org/10.1093/pcp/pcl040
Zhang MM, Zhang HK, Zhai JF, Zhang XS, Sang YL, Cheng ZJ (2021) ARF4 regulates shoot regeneration through coordination with ARF5 and IAA12. Plant Cell Rep 40:315–325. https://doi.org/10.1007/s00299-020-02633-w
Zhang TQ, Lian H, Zhou CM, Xu L, Jiao Y, Wang JW (2017) A two-step model for de novo activation of WUSCHEL during plant shoot regeneration. Plant Cell 29:1073–1087. https://doi.org/10.1105/tpc.16.00863
Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465:1089–1092. https://doi.org/10.1038/nature09126
Zhou JJ, Luo J (2018) The PIN-FORMED auxin efflux carriers in plants. Int J Mol Sci 19:2759. https://doi.org/10.3390/ijms19092759
Zubo YO, Blakley IC, Yamburenko MV, Worthen JM, Street IH, Franco-Zorrilla JM, Zhang W, Hill K, Raines T, Solano R, Kieber JJ, Loraine AE, Schaller GE (2017) Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in Arabidopsis. Proc Natl Acad Sci USA 114:5995–6004. https://doi.org/10.1073/pnas.1620749114
Zürcher E, Liu J, di Donato M, Geisler M, Müller B (2016) Plant development regulated by cytokinin sinks. Science 353:1027–1030. https://doi.org/10.1126/science.aaf7254
Acknowledgements
We are thankful to our colleague Dr. Slavica Ninković for the critical reading of the manuscript. The work of the authors is funded through the contract No. 451-03-9/2021-14/200007 of the Ministry of Education, Science and Technological Development of Republic of Serbia.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Ćosić, T., Raspor, M. (2022). The Role of Auxin and Cytokinin Signaling Components in de novo Shoot Organogenesis. In: Aftab, T. (eds) Auxins, Cytokinins and Gibberellins Signaling in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-031-05427-3_3
Download citation
DOI: https://doi.org/10.1007/978-3-031-05427-3_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-05426-6
Online ISBN: 978-3-031-05427-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)