Two principal growth regulators, cytokinins and ethylene, are known to interact in the regulation of plant growth. However, information about the underlying molecular mechanism and positional specificity of cytokinin/ethylene crosstalk in the control of root growth is scarce. We have identified the spatial specificity of cytokinin-regulated root elongation and root apical meristem (RAM) size, both of which we demonstrate to be dependent on ethylene biosynthesis. Upregulation of the cytokinin biosynthetic gene ISOPENTENYLTRANSFERASE (IPT) in proximal and peripheral tissues leads to both root and RAM shortening. By contrast, IPT activation in distal and inner tissues reduces RAM size while leaving the root length comparable to that of mock-treated controls. We show that cytokinins regulate two steps specific to ethylene biosynthesis: production of the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) by ACC SYNTHASEs (ACSs) and its conversion to ethylene by ACC OXIDASEs (ACOs). We describe cytokinin- and ethylene-specific regulation controlling the activity of ACSs and ACOs that are spatially discrete along both proximo/distal and radial root axes. Using direct ethylene measurements, we identify ACO2, ACO3, and ACO4 as being responsible for ethylene biosynthesis and ethylene-regulated root and RAM shortening in cytokinin-treated Arabidopsis. Direct interaction between ARABIDOPSIS RESPONSE REGULATOR 2 (ARR2), a member of the multistep phosphorelay cascade, and the C-terminal portion of ETHYLENE INSENSITIVE 2 (EIN2-C), a key regulator of canonical ethylene signaling, is involved in the cytokinin-induced, ethylene-mediated control of ACO4. We propose tight cooperation between cytokinin and ethylene signaling in the spatially specific regulation of ethylene biosynthesis as a key aspect of the hormonal control of root growth.

CEITEC Masaryk University Brno Czech Republic

CEITEC Masaryk University Brno Czech Republic; National Centre for Biomolecular Research Faculty of Science Masaryk University Brno Czech Republic

Center for Plant Molecular Biology University of Tübingen Tübingen Germany

Faculty of Science Palacký University and Institute of Experimental Botany The Czech Academy of Sciences Olomouc Czech Republic

Howard Hughes Medical Institute and Division of Biology and Biological Engineering California Institute of Technology Pasadena CA USA

Institute of Cytology and Genetics Siberian Branch Russian Academy of Sciences Novosibirsk 630090 Russia; Faculty of Natural Sciences Novosibirsk State University Novosibirsk 630090 Russia

Laboratory of Functional Plant Biology Department of Biology Ghent University Gent Belgium

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Bakker P., Pieterse C.M.J., de Jonge R., Berendsen R.L. The Soil-Borne Legacy. Cell. 2018;172:1178–1180. doi: 10.1016/j.cell.2018.02.024. PubMed DOI

Beemster G.T., Baskin T.I. Stunted plant 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. Plant Physiol. 2000;124:1718–1727. PubMed PMC

Bielach A., Podlesakova K., Marhavy P., Duclercq J., Cuesta C., Muller B., Grunewald W., Tarkowski P., Benkova E. Spatiotemporal regulation of lateral root organogenesis in Arabidopsis by cytokinin. Plant Cell. 2012;24:3967–3981. doi: 10.1105/tpc.112.103044. PubMed DOI PMC

Binder B.M. Ethylene signaling in plants. J. Biol. Chem. 2020;295:7710–7725. doi: 10.1074/jbc.REV120.010854. PubMed DOI PMC

Bohner S., Gatz C. Characterisation of novel target promoters for the dexamethasone-inducible/tetracycline-repressible regulator TGV using luciferase and isopentenyl transferase as sensitive reporter genes. Mol. Gen. Genet. 2001;264:860–870. doi: 10.1007/s004380000376. PubMed DOI

Brady S.M., Orlando D.A., Lee J.Y., Wang J.Y., Koch J., Dinneny J.R., Mace D., Ohler U., Benfey P.N. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science. 2007;318:801–806. doi: 10.1126/science.1146265. 318/5851/801 [pii] PubMed DOI

Cary A.J., Liu W., Howell S.H. Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol. 1995;107:1075–1082. 107/4/1075 [pii] PubMed PMC

Clough S.J., Bent A.F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. PubMed

Clouse R.M., Carraro N. A novel phylogeny and morphological reconstruction of the PIN genes and first phylogeny of the ACC-oxidases (ACOs) Front. Plant Sci. 2014;5:296. doi: 10.3389/fpls.2014.00296. PubMed DOI PMC

Comas L.H., Becker S.R., Cruz V.M., Byrne P.F., Dierig D.A. Root traits contributing to plant productivity under drought. Front. Plant Sci. 2013;4:442. doi: 10.3389/fpls.2013.00442. PubMed DOI PMC

Cortleven A., Leuendorf J.E., Frank M., Pezzetta D., Bolt S., Schmulling T. Cytokinin action in response to abiotic and biotic stresses in plants. Plant Cell Environ. 2019;42:998–1018. doi: 10.1111/pce.13494. PubMed DOI

Dello Ioio R., Linhares F.S., Scacchi E., Casamitjana-Martinez E., Heidstra R., Costantino P., Sabatini S. Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr. Biol. 2007;17:678–682. doi: 10.1016/j.cub.2007.02.047. S0960-9822(07)01056-1 [pii] PubMed DOI

Depaepe T., Van Der Straeten D. Tools of the Ethylene Trade: A Chemical Kit to Influence Ethylene Responses in Plants and Its Use in Agriculture. Small Methods. 2020;4 doi: 10.1002/smtd.201900267. DOI

Di Mambro R., Svolacchia N., Dello Ioio R., Pierdonati E., Salvi E., Pedrazzini E., Vitale A., Perilli S., Sozzani R., Benfey P.N., et al. The Lateral Root Cap Acts as an Auxin Sink that Controls Meristem Size. Curr. Biol. 2019;29:1199–1205.e4. doi: 10.1016/j.cub.2019.02.022. PubMed DOI

Dolan L. The role of ethylene in the development of plant form. J. Exp. Bot. 1997;48:201–210. doi: 10.1093/jxb/48.2.201. DOI

Etheridge N., Hall B.P., Schaller G.E. Progress report: ethylene signaling and responses. Planta. 2006;223:387–391. doi: 10.1007/s00425-005-0163-2. PubMed DOI

Hall B., Shakeel S., Amir M., Ul Haq N., Qu X., Schaller G.E. Histidine-Kinase Activity of the Ethylene Receptor ETR1 Facilitates the Ethylene Response in Arabidopsis. Plant Physiol. 2012;159:682–695. doi: 10.1104/pp.112.196790. PubMed DOI PMC

Hansen M., Chae H.S., Kieber J.J. Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J. 2009;57:606–614. doi: 10.1111/j.1365-313X.2008.03711.x. TPJ3711 [pii] PubMed DOI PMC

Hass C., Lohrmann J., Albrecht V., Sweere U., Hummel F., Yoo S.D., Hwang I., Zhu T., Schafer E., Kudla J. The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J. 2004;23:3290–3302. doi: 10.1038/sj.emboj.7600337. PubMed DOI PMC

Hetherington A.J., Dolan L. Bilaterally symmetric axes with rhizoids composed the rooting structure of the common ancestor of vascular plants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2018;373:20170042. doi: 10.1098/rstb.2017.0042. PubMed DOI PMC

Heyl A., Brault M., Frugier F., Kuderova A., Lindner A.C., Motyka V., Rashotte A.M., Schwartzenberg K.V., Vankova R., Schaller G.E. Nomenclature for members of the two-component signaling pathway of plants. Plant Physiol. 2013;161:1063–1065. doi: 10.1104/pp.112.213207. PubMed DOI PMC

Houben M., Van de Poel B. 1-Aminocyclopropane-1-Carboxylic Acid Oxidase (ACO): The Enzyme That Makes the Plant Hormone Ethylene. Front. Plant Sci. 2019;10:695. doi: 10.3389/fpls.2019.00695. PubMed DOI PMC

Hu Y.M., Vandenbussche F., Van Der Straeten D. Regulation of seedling growth by ethylene and the ethylene-auxin crosstalk. Planta. 2017;245:467–489. doi: 10.1007/s00425-017-2651-6. PubMed DOI

Chae H.S., Faure F., Kieber J.J. The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell. 2003;15:545–559. PubMed PMC

Chang J., Li X., Fu W., Wang J., Yong Y., Shi H., Ding Z., Kui H., Gou X., He K., Li J. Asymmetric distribution of cytokinins determines root hydrotropism in Arabidopsis thaliana. Cell Res. 2019;29:984–993. doi: 10.1038/s41422-019-0239-3. PubMed DOI PMC

Chen Y.F., Etheridge N., Schaller G.E. Ethylene signal transduction. Ann. Bot. 2005;95:901–915. doi: 10.1093/aob/mci100. mci100 [pii] PubMed DOI PMC

Ju C., Chang C. Advances in ethylene signalling: protein complexes at the endoplasmic reticulum membrane. AoB Plants. 2012;2012:pls031. doi: 10.1093/aobpla/pls031. PubMed DOI PMC

Karimi M., Depicker A., Hilson P. Recombinational cloning with plant gateway vectors. Plant Physiol. 2007;145:1144–1154. doi: 10.1104/pp.107.106989. PubMed DOI PMC

Kieber J.J., Schaller G.E. Cytokinin signaling in plant development. Development. 2018;145:dev149344. doi: 10.1242/dev.149344. PubMed DOI

Kieber J.J., Rothenberg M., Roman G., Feldmann K.A., Ecker J.R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993;72:427–441. 0092-8674(93)90119-B [pii] PubMed

Kong X., Liu G., Liu J., Ding Z. The Root Transition Zone: A Hot Spot for Signal Crosstalk. Trends Plant Sci. 2018;23:403–409. doi: 10.1016/j.tplants.2018.02.004. PubMed DOI

Kosakivska I.V., Vedenicheva N.P., Babenko L.M., Voytenko L.V., Romanenko K.O., Vasyuk V.A. Exogenous phytohormones in the regulation of growth and development of cereals under abiotic stresses. Mol. Biol. Rep. 2022;49:617–628. doi: 10.1007/s11033-021-06802-2. PubMed DOI

Laplaze L., Parizot B., Baker A., Ricaud L., Martiniere A., Auguy F., Franche C., Nussaume L., Bogusz D., Haseloff J. GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana. J. Exp. Bot. 2005;56:2433–2442. doi: 10.1093/jxb/eri236. eri236 [pii] PubMed DOI

Le J., Vandenbussche F., Van Der Straeten D., Verbelen J.P. In the early response of Arabidopsis roots to ethylene, cell elongation is up- and down-regulated and uncoupled from differentiation. Plant Physiol. 2001;125:519–522. PubMed PMC

Lee H.Y., Yoon G.M. Regulation of Ethylene Biosynthesis by Phytohormones in Etiolated Rice (Oryza sativa L.) Seedlings. Mol. Cells. 2018;41:311–319. doi: 10.14348/molcells.2018.2224. PubMed DOI PMC

Lee H.Y., Chen Y.C., Kieber J.J., Yoon G.M. Regulation of the turnover of ACC synthases by phytohormones and heterodimerization in Arabidopsis. Plant J. 2017;91:491–504. doi: 10.1111/tpj.13585. PubMed DOI

Leuendorf J.E., Schmuelling T. Meeting at the DNA: Specifying Cytokinin Responses through Transcription Factor Complex Formation. Plants-Basel. 2021;10 doi: 10.3390/plants10071458. PubMed DOI PMC

Li W., Ma M., Feng Y., Li H., Wang Y., Ma Y., Li M., An F., Guo H. EIN2-directed translational regulation of ethylene signaling in Arabidopsis. Cell. 2015;163:670–683. doi: 10.1016/j.cell.2015.09.037. PubMed DOI

Li W., Li Q., Lyu M., Wang Z., Song Z., Zhong S., Gu H., Dong J., Dresselhaus T., Zhong S., Qu L.J. Lack of ethylene does not affect reproductive success and synergid cell death in Arabidopsis. Mol. Plant. 2022;15:354–362. doi: 10.1016/j.molp.2021.11.001. PubMed DOI PMC

Liu S., Strauss S., Adibi M., Mosca G., Yoshida S., Dello Ioio R., Runions A., Andersen T.G., Grossmann G., Huijser P., et al. Cytokinin promotes growth cessation in the Arabidopsis root. Curr. Biol. 2022;32:1974–1985.e3. doi: 10.1016/j.cub.2022.03.019. PubMed DOI

Lynch J.P. Roots of the second green revolution. Aust. J. Bot. 2007;55:493–512. doi: 10.1071/Bt06118. DOI

Markakis M.N., De Cnodder T., Lewandowski M., Simon D., Boron A., Balcerowicz D., Doubbo T., Taconnat L., Renou J.P., Hofte H., et al. Identification of genes involved in the ACC-mediated control of root cell elongation in Arabidopsis thaliana. BMC Plant Biol. 2012;12:208. doi: 10.1186/1471-2229-12-208. PubMed DOI PMC

Mazzoni-Putman S.M., Brumos J., Zhao C., Alonso J.M., Stepanova A.N. Auxin Interactions with Other Hormones in Plant Development. Cold Spring Harb. Perspect. Biol. 2021;13:a039990. doi: 10.1101/cshperspect.a039990. PubMed DOI PMC

Mira-Rodado V. New Insights into Multistep-Phosphorelay (MSP)/Two-Component System (TCS) Regulation: Are Plants and Bacteria that Different? Plants. 2019;8:590. doi: 10.3390/plants8120590. PubMed DOI PMC

Miyawaki K., Matsumoto-Kitano M., Kakimoto T. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 2004;37:128–138. 1945 [pii] PubMed

Ortega-Martinez O., Pernas M., Carol R.J., Dolan L. Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science. 2007;317:507–510. doi: 10.1126/science.1143409. 317/5837/507 [pii] PubMed DOI

Pandey B.K., Huang G., Bhosale R., Hartman S., Sturrock C.J., Jose L., Martin O.C., Karady M., Voesenek L., Ljung K., et al. Plant roots sense soil compaction through restricted ethylene diffusion. Science. 2021;371:276–280. doi: 10.1126/science.abf3013. PubMed DOI

Park C.H., Roh J., Youn J.H., Son S.H., Park J.H., Kim S.Y., Kim T.W., Kim S.K. Arabidopsis ACC Oxidase 1 Coordinated by Multiple Signals Mediates Ethylene Biosynthesis and Is Involved in Root Development. Mol. Cells. 2018;41:923–932. doi: 10.14348/molcells.2018.0092. PubMed DOI PMC

Pattyn J., Vaughan-Hirsch J., Van de Poel B. The regulation of ethylene biosynthesis: a complex multilevel control circuitry. New Phytol. 2021;229:770–782. doi: 10.1111/nph.16873. PubMed DOI PMC

Ramireddy E., Hosseini S.A., Eggert K., Gillandt S., Gnad H., von Wiren N., Schmulling T. Root Engineering in Barley: Increasing Cytokinin Degradation Produces a Larger Root System, Mineral Enrichment in the Shoot and Improved Drought Tolerance. Plant Physiol. 2018;177:1078–1095. doi: 10.1104/pp.18.00199. PubMed DOI PMC

Rashotte A.M., Chae H.S., Maxwell B.B., Kieber J.J. The interaction of cytokinin with other signals. Physiol. Plantarum. 2005;123:184–194. doi: 10.1111/j.1399-3054.2004.00445.x. DOI

Rieger J., Fitz M., Fischer S.M., Wallmeroth N., Flores-Romero H., Fischer N.M., Brand L.H., Garcia-Saez A.J., Berendzen K.W., Mira-Rodado V. Exploring the Binding Affinity of the ARR2 GARP DNA Binding Domain via Comparative Methods. Genes. 2023;14:1638. doi: 10.3390/genes14081638. PubMed DOI PMC

Ruzicka K., Ljung K., Vanneste S., Podhorska R., Beeckman T., Friml J., Benkova E. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell. 2007;19:2197–2212. doi: 10.1105/tpc.107.052126. tpc.107.052126 [pii] PubMed DOI PMC

Ruzicka K., Simaskova M., Duclercq J., Petrasek J., Zazimalova E., Simon S., Friml J., Van Montagu M.C., Benkova E. Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc. Natl. Acad. Sci. USA. 2009;106:4284–4289. doi: 10.1073/pnas.0900060106. 0900060106 [pii] PubMed DOI PMC

Sakai H., Aoyama T., Oka A. Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 2000;24:703–711. PubMed

Satoh S., Esashi Y. Effects of alpha-aminoisobutyric acid and D- and L-amino acids on ethylene production and content of 1-aminocyclopropane-1-carboxylic acid in cotyledonary segments of cocklebur seeds. Physiol. Plant. 1982;54:147–152. doi: 10.1111/j.1399-3054.1982.tb06318.x. DOI

Satoh S., Esashi Y. α-Aminoisabutyric acid, propyl gallate and cobalt ion and the mode of inhibition of ethylene production by cotyledonary segments of cocklebur seeds. Physiol. Plant. 1983;57:521–526. doi: 10.1111/j.1399-3054.1983.tb02779.x. DOI

Saucedo M., Ponce G., Campos M.E., Eapen D., Garcia E., Lujan R., Sanchez Y., Cassab G.I. An altered hydrotropic response (ahr1) mutant of Arabidopsis recovers root hydrotropism with cytokinin. J. Exp. Bot. 2012;63:3587–3601. doi: 10.1093/jxb/ers025. PubMed DOI PMC

Shimada T.L., Shimada T., Hara-Nishimura I. A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 2010;61:519–528. doi: 10.1111/j.1365-313X.2009.04060.x. PubMed DOI

Skalak J., Nicolas K.L., Vankova R., Hejatko J. Signal Integration in Plant Abiotic Stress Responses via Multistep Phosphorelay Signaling. Front. Plant Sci. 2021;12:644823. doi: 10.3389/fpls.2021.644823. PubMed DOI PMC

Stepanova A.N., Alonso J.M. Ethylene signaling and response: where different regulatory modules meet. Curr. Opin. Plant Biol. 2009;12:548–555. doi: 10.1016/j.pbi.2009.07.009. PubMed DOI

Stepanova A.N., Robertson-Hoyt J., Yun J., Benavente J.M., Xie D.Y., Dolezal K., Schlereth A., Jurgens G., Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 2008;133:177–191. doi: 10.1016/j.cell.2008.01.047. PubMed DOI

Street I.H., Aman S., Zubo Y., Ramzan A., Wang X., Shakeel S., Kieber J.J., Schaller G.E. Ethylene Inhibits Cell Proliferation of the Arabidopsis Root Meristem. Plant Physiol. 2015;169:338–350. doi: 10.1104/pp.15.00415. PubMed DOI PMC

Street I.H., Mathews D.E., Yamburkenko M.V., Sorooshzadeh A., John R.T., Swarup R., Bennett M.J., Kieber J.J., Schaller G.E. Cytokinin acts through the auxin influx carrier AUX1 to regulate cell elongation in the root. Development. 2016;143:3982–3993. doi: 10.1242/dev.132035. PubMed DOI PMC

Sun X., Li Y., He W., Ji C., Xia P., Wang Y., Du S., Li H., Raikhel N., Xiao J., Guo H. Pyrazinamide and derivatives block ethylene biosynthesis by inhibiting ACC oxidase. Nat. Commun. 2017;8:15758. doi: 10.1038/ncomms15758. PubMed DOI PMC

Svolacchia N., Salvi E., Sabatini S. Arabidopsis primary root growth: let it grow, can't hold it back anymore. Curr. Opin. Plant Biol. 2020;57:133–141. doi: 10.1016/j.pbi.2020.08.005. PubMed DOI

Swarup R., Perry P., Hagenbeek D., Van Der Straeten D., Beemster G.T., Sandberg G., Bhalerao R., Ljung K., Bennett M.J. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell. 2007;19:2186–2196. doi: 10.1105/tpc.107.052100. tpc.107.052100 [pii] PubMed DOI PMC

Szmitkowska A., Cuyacot A.R., Pekarova B., Zdarska M., Houser J., Komarek J., Jasenakova Z., Jayasree A., Heunemann M., Ubogoeva E., et al. AHK5 mediates ETR1-initiated multistep phosphorelay in Arabidopsis. bioRxiv. 2021 doi: 10.1101/2021.09.16.460643. Preprint at. DOI

Takatsuka H., Umeda M. Hormonal control of cell division and elongation along differentiation trajectories in roots. J. Exp. Bot. 2014;65:2633–2643. doi: 10.1093/jxb/ert485. PubMed DOI

Tiwari M., Kumar R., Min D., Jagadish S.V.K. Genetic and molecular mechanisms underlying root architecture and function under heat stress-A hidden story. Plant Cell Environ. 2022;45:771–788. doi: 10.1111/pce.14266. PubMed DOI

Tsuchisaka A., Theologis A. Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol. 2004;136:2982–3000. doi: 10.1104/pp.104.049999. 49999 [pii] PubMed DOI PMC

Tsuchisaka A., Yu G., Jin H., Alonso J.M., Ecker J.R., Zhang X., Gao S., Theologis A. A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics. 2009;183:979–1003. doi: 10.1534/genetics.109.107102. PubMed DOI PMC

Uga Y., Sugimoto K., Ogawa S., Rane J., Ishitani M., Hara N., Kitomi Y., Inukai Y., Ono K., Kanno N., et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet. 2013;45:1097–1102. doi: 10.1038/ng.2725. PubMed DOI

Vandenbussche F., Vaseva I., Vissenberg K., Van Der Straeten D. Ethylene in vegetative development: a tale with a riddle. New Phytol. 2012;194:895–909. doi: 10.1111/j.1469-8137.2012.04100.x. PubMed DOI

Vaseva I.I., Qudeimat E., Potuschak T., Du Y., Genschik P., Vandenbussche F., Van Der Straeten D. The plant hormone ethylene restricts Arabidopsis growth via the epidermis. Proc. Natl. Acad. Sci. USA. 2018;115:E4130–E4139. doi: 10.1073/pnas.1717649115. PubMed DOI PMC

Venado R.E., Wange L.E., Shen D., Pinnau F., Andersen T.G., Enard W., Marin M. Tissue-specific regulation of lipid polyester synthesis genes controlling oxygen permeation into Lotus japonicus nodules. Proc. Natl. Acad. Sci. USA. 2022;119 doi: 10.1073/pnas.2206291119. PubMed DOI PMC

Vogel J.P., Woeste K.E., Theologis A., Kieber J.J. Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl. Acad. Sci. USA. 1998;95:4766–4771. PubMed PMC

Waidmann S., Kleine-Vehn J. Asymmetric cytokinin signaling opposes gravitropism in roots. J. Integr. Plant Biol. 2020;62:882–886. doi: 10.1111/jipb.12929. PubMed DOI PMC

Waidmann S., Ruiz Rosquete M., Scholler M., Sarkel E., Lindner H., LaRue T., Petrik I., Dunser K., Martopawiro S., Sasidharan R., et al. Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots. Nat. Commun. 2019;10:3540. doi: 10.1038/s41467-019-11483-4. PubMed DOI PMC

Wang L., Zhang F., Rode S., Chin K.K., Ko E.E., Kim J., Iyer V.R., Qiao H. Ethylene induces combinatorial effects of histone H3 acetylation in gene expression in Arabidopsis. BMC Genom. 2017;18:538. doi: 10.1186/s12864-017-3929-6. PubMed DOI PMC

Weits D.A., Kunkowska A.B., Kamps N.C.W., Portz K.M.S., Packbier N.K., Nemec Venza Z., Gaillochet C., Lohmann J.U., Pedersen O., van Dongen J.T., Licausi F. An apical hypoxic niche sets the pace of shoot meristem activity. Nature. 2019;569:714–717. doi: 10.1038/s41586-019-1203-6. PubMed DOI

Wen X., Zhang C., Ji Y., Zhao Q., He W., An F., Jiang L., Guo H. Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Res. 2012;22:1613–1616. doi: 10.1038/cr.2012.145. PubMed DOI PMC

Woeste K.E., Ye C., Kieber J.J. Two Arabidopsis mutants that overproduce ethylene are affected in the posttranscriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase. Plant Physiol. 1999;119:521–530. PubMed PMC

Yamoune A., Cuyacot A.R., Zdarska M., Hejatko J. Hormonal orchestration of root apical meristem formation and maintenance in Arabidopsis. J. Exp. Bot. 2021;72:6768–6788. doi: 10.1093/jxb/erab360. PubMed DOI

Yang S.F., Hoffman N.E. Ethylene Biosynthesis and Its Regulation in Higher-Plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1984;35:155–189.

Yang Y., Li R., Qi M. In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J. 2000;22:543–551. doi: 10.1046/j.1365-313x.2000.00760.x. PubMed DOI

Zd'arska M., Zatloukalova P., Benitez M., Sedo O., Potesil D., Novak O., Svacinova J., Pesek B., Malbeck J., Vasickova J., et al. Proteome analysis in Arabidopsis reveals shoot- and root-specific targets of cytokinin action and differential regulation of hormonal homeostasis. Plant Physiology. 2013;161:918–930. doi: 10.1104/pp.112.202853. PubMed DOI PMC

Zdarska M., Cuyacot A.R., Tarr P.T., Yamoune A., Szmitkowska A., Hrdinova V., Gelova Z., Meyerowitz E.M., Hejatko J. ETR1 Integrates Response to Ethylene and Cytokinins into a Single Multistep Phosphorelay Pathway to Control Root Growth. Mol. Plant. 2019;12:1338–1352. doi: 10.1016/j.molp.2019.05.012. PubMed DOI PMC

Zemlyanskaya E.V., Omelyanchuk N.A., Ubogoeva E.V., Mironova V.V. Deciphering Auxin-Ethylene Crosstalk at a Systems Level. Int. J. Mol. Sci. 2018;19 doi: 10.3390/ijms19124060. PubMed DOI PMC

Zhang F., Qi B., Wang L., Zhao B., Rode S., Riggan N.D., Ecker J.R., Qiao H. EIN2-dependent regulation of acetylation of histone H3K14 and non-canonical histone H3K23 in ethylene signalling. Nat. Commun. 2016;7:13018. doi: 10.1038/ncomms13018. PubMed DOI PMC

Zhang F., Wang L., Qi B., Zhao B., Ko E.E., Riggan N.D., Chin K., Qiao H. EIN2 mediates direct regulation of histone acetylation in the ethylene response. Proc. Natl. Acad. Sci. USA. 2017;114:10274–10279. doi: 10.1073/pnas.1707937114. PubMed DOI PMC

Zhang Z., Zhang H., Quan R., Wang X.C., Huang R. Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol. 2009;150:365–377. doi: 10.1104/pp.109.135830. PubMed DOI PMC

Zhao H., Duan K.X., Ma B., Yin C.C., Hu Y., Tao J.J., Huang Y.H., Cao W.Q., Chen H., Yang C., et al. Histidine kinase MHZ1/OsHK1 interacts with ethylene receptors to regulate root growth in rice. Nat. Commun. 2020;11:518. doi: 10.1038/s41467-020-14313-0. PubMed DOI PMC

Zou X., Shao J., Wang Q., Chen P., Zhu Y., Yin C. Supraoptimal Cytokinin Content Inhibits Rice Seminal Root Growth by Reducing Root Meristem Size and Cell Length via Increased Ethylene Content. Int. J. Mol. Sci. 2018;19:4051. 3390/ijms19124051. PubMed PMC

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