Plant hormones are master regulators of plant growth and development. Better knowledge of their spatial signaling and homeostasis (transport and metabolism) on the lowest structural levels (cellular and subcellular) is therefore crucial to a better understanding of developmental processes in plants. Recent progress in phytohormone analysis at the cellular and subcellular levels has greatly improved the effectiveness of isolation protocols and the sensitivity of analytical methods. This review is mainly focused on homeostasis of two plant hormone groups, auxins and cytokinins. It will summarize and discuss their tissue- and cell-type specific distributions at the cellular and subcellular levels.

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science of Palacký University Šlechtitelů 27 78371 Olomouc Czech Republic

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Institute of Experimental Botany of the Czech Academy of Sciences and Faculty of Science of Palacký University Šlechtitelů 27 78371 Olomouc Czech Republic

School of Life Sciences University of Warwick Coventry CV4 7AL UK

Zobrazit více v PubMed

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

Müller B., Sheen J. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature. 2008;453:1094–1097. doi: 10.1038/nature06943. PubMed DOI PMC

Efroni I., Mello A., Nawy T., Ip P.-L., Rahni R., DelRose N., Powers A., Satija R., Birnbaum K.D. Root regeneration triggers an embryo-like sequence guided by hormonal interactions. Cell. 2016;165:1721–1733. doi: 10.1016/j.cell.2016.04.046. 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

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

Novák O., Napier R., Ljung K. Zooming In on Plant Hormone Analysis: Tissue- and Cell-Specific Approaches. Annu. Rev. Plant Biol. 2017;68:323–348. doi: 10.1146/annurev-arplant-042916-040812. PubMed DOI

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

De Duve C., Pressman B.C., Gianetto R., Wattiaux R., Appelmans F. Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem. J. 1955;60:604–617. doi: 10.1042/bj0600604. PubMed DOI PMC

Huber L.A., Pfaller K., Vietor I. Organelle Proteomics: Implications for Subcellular Fractionation in Proteomics. Circ. Res. 2003;92:962–968. doi: 10.1161/01.RES.0000071748.48338.25. PubMed DOI

Robert S., Zouhar J., Carter C.J., Raikhel N. Isolation of intact vacuoles from Arabidopsis rosette leaf–derived protoplasts. Nat. Protoc. 2007;2:259–262. doi: 10.1038/nprot.2007.26. PubMed DOI

Seigneurin-Berny D., Salvi D., Dorne A.-J., Joyard J., Rolland N. Percoll-purified and photosynthetically active chloroplasts from Arabidopsis thaliana leaves. Plant Physiol. Biochem. 2008;46:951–955. doi: 10.1016/j.plaphy.2008.06.009. PubMed DOI

Wulfetange K., Lomin S.N., Romanov G.A., Stolz A., Heyl A., Schmülling T. The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol. 2011;156:1808–1818. doi: 10.1104/pp.111.180539. PubMed DOI PMC

Ding Z., Wang B., Moreno I., Dupláková N., Simon S., Carraro N., Reemmer J., Pěnčík A., Chen X., Tejos R., et al. ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat. Commun. 2012;3:941. doi: 10.1038/ncomms1941. PubMed DOI

Somerville C.R., Somerville S.C., Ogren W.L. Isolation of photosynthetically active protoplasts and chloroplastids from Arabidopsis thaliana. Plant Sci. Lett. 1981;21:89–96. doi: 10.1016/0304-4211(81)90073-0. DOI

Keech O., Dizengremel P., Gardeström P. Preparation of leaf mitochondria from Arabidopsis thaliana. Physiol. Plant. 2005;124:403–409. doi: 10.1111/j.1399-3054.2005.00521.x. DOI

Parsons H.T., Christiansen K., Knierim B., Carroll A., Ito J., Batth T.S., Smith-Moritz A.M., Morrison S., McInerney P., Hadi M.Z., et al. Isolation and Proteomic Characterization of the Arabidopsis Golgi Defines Functional and Novel Components Involved in Plant Cell Wall Biosynthesis. Plant Physiol. 2012;159:12–26. doi: 10.1104/pp.111.193151. PubMed DOI PMC

Kriechbaumer V., Wang P., Hawes C., Abell B.M. Alternative splicing of the auxin biosynthesis gene YUCCA4 determines its subcellular compartmentation. Plant J. 2012;70:292–302. doi: 10.1111/j.1365-313X.2011.04866.x. PubMed DOI

Minami A., Takahashi D., Kawamura Y., Uemura M. Methods in Molecular Biology. Volume 1511. Human Press; Clifton, NJ, USA: 2017. Isolation of plasma membrane and plasma membrane microdomains; pp. 199–212. PubMed

Fürtauer L., Weckwerth W., Nägele T. A Benchtop Fractionation Procedure for Subcellular Analysis of the Plant Metabolome. Front. Plant Sci. 2016;7:1912. doi: 10.3389/fpls.2016.01912. PubMed DOI PMC

Dietz K.-J. Subcellular metabolomics: The choice of method depends on the aim of the study. J. Exp. Bot. 2017;68:5695–5698. doi: 10.1093/jxb/erx406. PubMed DOI PMC

Petrovská B., Jeřábková H., Chamrád I., Vrána J., Lenobel R., Uřinovská J., Šebela M., Doležel J. Proteomic analysis of barley cell nuclei purified by flow sorting. Cytogenet. Genome Res. 2014;143:78–86. doi: 10.1159/000365311. PubMed DOI

Wolf P.G., Karol K.G., Mandoli D.F., Kuehl J., Arumuganathan K., Ellis M.W., Mishler B.D., Kelch D.G., Olmstead R.G., Boore J.L. The first complete chloroplast genome sequence of a lycophyte, Huperzia lucidula (Lycopodiaceae) Gene. 2005;350:117–128. doi: 10.1016/j.gene.2005.01.018. PubMed DOI

Cossarizza A., Ceccarelli D., Masini A. Functional heterogeneity of an isolated mitochondrial population revealed by cytofluorometric analysis at the single organelle level. Exp. Cell Res. 1996;222:84–94. doi: 10.1006/excr.1996.0011. PubMed DOI

Deal R.B., Henikoff S. The INTACT method for cell type–specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat. Protoc. 2011;6:56–68. doi: 10.1038/nprot.2010.175. PubMed DOI PMC

Chen W.W., Freinkman E., Wang T., Birsoy K., Sabatini D.M. Absolute Quantification of Matrix Metabolites reveals the dynamics of mitochondrial metabolism. Cell. 2016;166:1324–1337. doi: 10.1016/j.cell.2016.07.040. PubMed DOI PMC

Sandberg G., Gardeström P., Sitbon F., Olsson O. Presence of indole-3-acetic acid in chloroplasts of Nicotiana tabacum and Pinus sylvestris. Planta. 1990;180:562–568. doi: 10.1007/BF02411455. PubMed DOI

Benková E., Witters E., Van Dongen W., Kolář J., Motyka V., Brzobohatý B., Van Onckelen H.A., Macháčková I. Cytokinins in tobacco and wheat chloroplasts. Occurrence and changes due to light/dark treatment. Plant Physiol. 1999;121:245–252. doi: 10.1104/pp.121.1.245. PubMed DOI PMC

Polanská L., Vičánková A., Nováková M., Malbeck J., Dobrev P.I., Brzobohatý B., Vaňková R., Macháčková I. Altered cytokinin metabolism affects cytokinin, auxin, and abscisic acid contents in leaves and chloroplasts, and chloroplast ultrastructure in transgenic tobacco. J. Exp. Bot. 2007;58:637–649. doi: 10.1093/jxb/erl235. PubMed DOI

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 homoeostasis. Nat. Commun. 2013;4:2625. doi: 10.1038/ncomms3625. PubMed DOI PMC

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

Svačinová J., Novák O., Plačková L., Lenobel R., Holík J., Strnad M., Doležal K. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: Pipette tip solid-phase extraction. Plant Methods. 2012;8:17. doi: 10.1186/1746-4811-8-17. PubMed DOI PMC

Pěnčík A., Simonovik B., Petersson S.V., Henyková E., Simon S., Greenham K., Zhang Y., Kowalczyk M., Estelle M., Zažímalová E., et al. Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid. Plant Cell. 2013;25:3858–3870. doi: 10.1105/tpc.113.114421. PubMed DOI PMC

Novák O., Hényková E., Sairanen I., Kowalczyk M., Pospíšil T., Ljung K. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 2012;72:523–536. doi: 10.1111/j.1365-313X.2012.05085.x. PubMed DOI

Korasick D.A., Enders T.A., Strader L.C. Auxin biosynthesis and storage forms. J. Exp. Bot. 2013;64:2541–2555. doi: 10.1093/jxb/ert080. PubMed DOI PMC

Grones P., Friml J. Auxin transporters and binding proteins at a glance. J. Cell Sci. 2015;128:1–7. doi: 10.1242/jcs.159418. PubMed DOI

Strader L.C., Zhao Y. Auxin perception and downstream events. Curr. Opin. Plant Biol. 2016;33:8–14. doi: 10.1016/j.pbi.2016.04.004. PubMed DOI PMC

Ganguly A., Sasayama D., Cho H.-T. Regulation of the polarity of protein trafficking by phosphorylation. Mol. Cells. 2012;33:423–430. doi: 10.1007/s10059-012-0039-9. PubMed DOI PMC

Friml J. Auxin transport—Shaping the plant. Curr. Opin. Plant Biol. 2003;6:7–12. doi: 10.1016/S1369526602000031. PubMed DOI

Ljung K. Auxin metabolism and homeostasis during plant development. Development. 2013;140:943–950. doi: 10.1242/dev.086363. PubMed DOI

Zolman B.K., Martinez N., Millius A., Adham A.R., Bartel B. Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes. Genetics. 2008;180:237–251. doi: 10.1534/genetics.108.090399. PubMed DOI PMC

Liu X., Hegeman A.D., Gardner G., Cohen J.D. Protocol: High-throughput and quantitative assays of auxin and auxin precursors from minute tissue samples. Plant Methods. 2012;8:31. doi: 10.1186/1746-4811-8-31. PubMed DOI PMC

Lee S., Sundaram S., Armitage L., Evans J.P., Hawkes T., Kepinski S., Ferro N., Napier R. Defining binding efficiency and specificity of auxins for SCF(TIR1/AFB)-Aux/IAA co-receptor complex formation. ACS Chem. Biol. 2014;9:673–682. doi: 10.1021/cb400618m. PubMed DOI PMC

Uzunova V.V., Quareshy M., Del Genio C.I., Napier R. Tomographic docking suggests the mechanism of auxin receptor TIR1 selectivity. Open Biol. 2016;6:160139. doi: 10.1098/rsob.160139. PubMed DOI PMC

Frick E.M., Strader L.C. Roles for IBA-derived auxin in plant development. J. Exp. Bot. 2018;69:169–177. doi: 10.1093/jxb/erx298. PubMed DOI PMC

Woodward A.W., Bartel B. Auxin: Regulation, action, and interaction. Ann. Bot. 2005;95:707–735. doi: 10.1093/aob/mci083. PubMed DOI PMC

Mashiguchi K., Tanaka K., Sakai T., Sugawara S., Kawaide H., Natsume M., Hanada A., Yaeno T., Shirasu K., Yao H., et al. The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2011;108:18512–18517. doi: 10.1073/pnas.1108434108. PubMed DOI PMC

Spaepen S., Vanderleyden J., Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 2007;31:425–448. doi: 10.1111/j.1574-6976.2007.00072.x. PubMed DOI

Nonhebel H.M. Tryptophan-independent indole-3-acetic acid synthesis: Critical evaluation of the evidence. Plant Physiol. 2015;169:1001–1005. doi: 10.1104/pp.15.01091. PubMed DOI PMC

Wang B., Chu J., Yu T., Xu Q., Sun X., Yuan J., Xiong G., Wang G., Wang Y., Li J. Tryptophan-independent auxin biosynthesis contributes to early embryogenesis in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2015;112:4821–4826. doi: 10.1073/pnas.1503998112. PubMed DOI PMC

Zhao Y., Christensen S.K., Fankhauser C., Cashman J.R., Cohen J.D., Weigel D., Chory J. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science. 2001;291:306–309. doi: 10.1126/science.291.5502.306. PubMed DOI

Stepanova A.N., Yun J., Robles L.M., Novák O., He W., Guo H., Ljung K., Alonso J.M. The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell. 2011;23:3961–3973. doi: 10.1105/tpc.111.088047. PubMed DOI PMC

Kriechbaumer V., Seo H., Park W.J., Hawes C. Endoplasmic reticulum localization and activity of maize auxin biosynthetic enzymes. J. Exp. Bot. 2015;66:6009–6020. doi: 10.1093/jxb/erv314. PubMed DOI

Hull A.K., Vij R., Celenza J.L. Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc. Natl. Acad. Sci. USA. 2000;97:2379–2384. doi: 10.1073/pnas.040569997. PubMed DOI PMC

Zhao Y., Hull A.K., Gupta N.R., Goss K.A., Alonso J.M., Ecker J.R., Normanly J., Chory J., Celenza J.L. Trp-dependent auxin biosynthesis in Arabidopsis: Involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev. 2002;16:3100–3112. doi: 10.1101/gad.1035402. PubMed DOI PMC

Sugawara S., Hishiyama S., Jikumaru Y., Hanada A., Nishimura T., Koshiba T., Zhao Y., Kamiya Y., Kasahara H. Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2009;106:5430–5435. doi: 10.1073/pnas.0811226106. PubMed DOI PMC

Pollmann S., Neu D., Lehmann T., Berkowitz O., Schäfer T., Weiler E.W. Subcellular localization and tissue specific expression of amidase 1 from Arabidopsis thaliana. Planta. 2006;224:1241–1253. doi: 10.1007/s00425-006-0304-2. PubMed DOI

Nemoto K., Hara M., Suzuki M., Seki H., Muranaka T., Mano Y. The NtAMI1 gene functions in cell division of tobacco BY-2 cells in the presence of indole-3-acetamide. FEBS Lett. 2009;583:487–492. doi: 10.1016/j.febslet.2008.12.049. PubMed DOI

Ludwig-Müller J. Auxin conjugates: Their role for plant development and in the evolution of land plants. J. Exp. Bot. 2011;62:1757–1773. doi: 10.1093/jxb/erq412. PubMed DOI

Mano Y., Nemoto K. The pathway of auxin biosynthesis in plants. J. Exp. Bot. 2012;63:2853–2872. doi: 10.1093/jxb/ers091. PubMed DOI

Zhang J., Peer W.A. Auxin homeostasis: The DAO of catabolism. J. Exp. Bot. 2017;68:3145–3154. doi: 10.1093/jxb/erx221. PubMed DOI

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

Petrášek J., Friml J. Auxin transport routes in plant development. Development. 2009;136:2675–2688. doi: 10.1242/dev.030353. PubMed DOI

Verrier P.J., Bird D., Burla B., Dassa E., Forestier C., Geisler M., Klein M., Kolukisaoglu H.U., Lee Y., Martinoia E., et al. Plant ABC proteins—A unified nomenclature and updated inventory. Trends Plant Sci. 2008;13:151–159. doi: 10.1016/j.tplants.2008.02.001. PubMed DOI

Yang H., Murphy A.S. Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J. 2009;59:179–191. doi: 10.1111/j.1365-313X.2009.03856.x. PubMed DOI

Kubeš M., Yang H., Richter G.L., Cheng Y., Młodzińska E., Wang X., Blakeslee J.J., Carraro N., Petrášek J., Zažímalová E., et al. The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J. 2012;69:640–654. doi: 10.1111/j.1365-313X.2011.04818.x. 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

Gojon A., Krouk G., Perrine-Walker F., Laugier E. Nitrate transceptor(s) in plants. J. Exp. Bot. 2011;62:2299–2308. doi: 10.1093/jxb/erq419. PubMed DOI

Corratgé-Faillie C., Lacombe B. Substrate (un)specificity of Arabidopsis NRT1/PTR FAMILY (NPF) proteins. J. Exp. Bot. 2017;68:3107–3113. doi: 10.1093/jxb/erw499. PubMed DOI

Powers S.K., Strader L.C. Up in the air: Untethered Factors of Auxin Response. F1000Research. 2016;5 doi: 10.12688/f1000research.7492.1. PubMed DOI PMC

Jin S.-H., Ma X.-M., Han P., Wang B., Sun Y.-G., Zhang G.-Z., Li Y.-J., Hou B.-K. UGT74D1 is a novel auxin glycosyltransferase from Arabidopsis thaliana. PLoS ONE. 2013;8:e61705. doi: 10.1371/annotation/457d7567-fc12-421c-9d79-880950ab10e1. PubMed DOI PMC

Staswick P.E., Serban B., Rowe M., Tiryaki I., Maldonado M.T., Maldonado M.C., Suza W. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell. 2005;17:616–627. doi: 10.1105/tpc.104.026690. PubMed DOI PMC

Cano A., Sánchez-García A.B., Albacete A., González-Bayón R., Justamante M.S., Ibáñez S., Acosta M., Pérez-Pérez J.M. Enhanced conjugation of auxin by GH3 enzymes leads to poor adventitious rooting in carnation stem cuttings. Front. Plant Sci. 2018;9 doi: 10.3389/fpls.2018.00566. PubMed DOI PMC

Barbez E., Kleine-Vehn J. Divide Et Impera—cellular auxin compartmentalization. Curr. Opin. Plant Biol. 2013;16:78–84. doi: 10.1016/j.pbi.2012.10.005. PubMed DOI

LeClere S., Tellez R., Rampey R.A., Matsuda S.P.T., Bartel B. Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J. Biol. Chem. 2002;277:20446–20452. doi: 10.1074/jbc.M111955200. PubMed DOI

Okrent R.A., Brooks M.D., Wildermuth M.C. Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate. J. Biol. Chem. 2009;284:9742–9754. doi: 10.1074/jbc.M806662200. PubMed DOI PMC

Chen Q., Westfall C.S., Hicks L.M., Wang S., Jez J.M. Kinetic basis for the conjugation of auxin by a GH3 family indole-acetic acid-amido synthetase. J. Biol. Chem. 2010;285:29780–29786. doi: 10.1074/jbc.M110.146431. PubMed DOI PMC

Kramer E.M., Ackelsberg E.M. Auxin metabolism rates and implications for plant development. Front. Plant Sci. 2015;6:150. doi: 10.3389/fpls.2015.00150. PubMed DOI PMC

Westfall C.S., Sherp A.M., Zubieta C., Alvarez S., Schraft E., Marcellin R., Ramirez L., Jez J.M. Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis. Proc. Natl. Acad. Sci. USA. 2016;113:13917–13922. doi: 10.1073/pnas.1612635113. PubMed DOI PMC

Ostin A., Kowalczyk M., Bhalerao R., Sandberg G. Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol. 1998;118:285–296. doi: 10.1104/pp.118.1.285. PubMed DOI PMC

Kowalczyk M., Sandberg G. Quantitative analysis of indole-3-acetic acid metabolites in Arabidopsis. Plant Physiol. 2001;127:1845–1853. doi: 10.1104/pp.010525. PubMed DOI PMC

Tanaka K., Hayashi K., Natsume M., Kamiya Y., Sakakibara H., Kawaide H., Kasahara H. UGT74D1 catalyzes the glucosylation of 2-oxindole-3-acetic acid in the auxin metabolic pathway in Arabidopsis. Plant Cell Physiol. 2014;55:218–228. doi: 10.1093/pcp/pct173. PubMed DOI PMC

Porco S., Pěnčík A., Rashed A., Voß U., Casanova-Sáez R., Bishopp A., Golebiowska A., Bhosale R., Swarup R., Swarup K., et al. Dioxygenase-encoding AtDAO1 gene controls IAA oxidation and homeostasis in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2016;113:11016–11021. doi: 10.1073/pnas.1604375113. PubMed DOI PMC

Kai K., Horita J., Wakasa K., Miyagawa H. Three oxidative metabolites of indole-3-acetic acid from Arabidopsis thaliana. Phytochemistry. 2007;68:1651–1663. doi: 10.1016/j.phytochem.2007.04.030. PubMed DOI

Zhao Z., Zhang Y., Liu X., Zhang X., Liu S., Yu X., Ren Y., Zheng X., Zhou K., Jiang L., et al. A role for a dioxygenase in auxin metabolism and reproductive development in rice. Dev. Cell. 2013;27:113–122. doi: 10.1016/j.devcel.2013.09.005. PubMed DOI

Zhang J., Lin J.E., Harris C., Campos Mastrotti Pereira F., Wu F., Blakeslee J.J., Peer W.A. DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 2016;113:11010–11015. doi: 10.1073/pnas.1604769113. PubMed DOI PMC

Mellor N., Band L.R., Pěnčík A., Novák O., Rashed A., Holman T., Wilson M.H., Voß U., Bishopp A., King J.R., et al. Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. Proc. Natl. Acad. Sci. USA. 2016;113:11022–11027. doi: 10.1073/pnas.1604458113. PubMed DOI PMC

Qin G., Gu H., Zhao Y., Ma Z., Shi G., Yang Y., Pichersky E., Chen H., Liu M., Chen Z., et al. An Indole-3-Acetic Acid Carboxyl Methyltransferase Regulates Arabidopsis Leaf Development. Plant Cell. 2005;17:2693–2704. doi: 10.1105/tpc.105.034959. PubMed DOI PMC

Abbas M., Hernández-García J., Pollmann S., Samodelov S.L., Kolb M., Friml J., Hammes U.Z., Zurbriggen M.D., Blázquez M.A., Alabadí D. Auxin methylation is required for differential growth in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2018;115:6864–6869. doi: 10.1073/pnas.1806565115. PubMed DOI PMC

Stepanova A.N., Alonso J.M. Auxin catabolism unplugged: Role of IAA oxidation in auxin homeostasis. Proc. Natl. Acad. Sci. USA. 2016;113:10742–10744. doi: 10.1073/pnas.1613506113. PubMed DOI PMC

Swarup R., Friml J., Marchant A., Ljung K., Sandberg G., Palme K., Bennett M. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev. 2001;15:2648–2653. doi: 10.1101/gad.210501. 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

Krouk G., Lacombe B., Bielach A., Perrine-Walker F., Malinska K., Mounier E., Hoyerová 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

Bouguyon E., Brun F., Meynard D., Kubeš M., Pervent M., Leran S., Lacombe B., Krouk G., Guiderdoni E., Zažímalová E., et al. Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. plants. 2015;1:15015. doi: 10.1038/nplants.2015.15. PubMed DOI

Krouk G. Hormones and nitrate: A two-way connection. Plant Mol. Biol. 2016;91:599–606. doi: 10.1007/s11103-016-0463-x. PubMed DOI

Li R., Li J., Li S., Qin G., Novák O., Pěnčík A., Ljung K., Aoyama T., Liu J., Murphy A.S., et al. ADP1 affects plant architecture by regulating local auxin biosynthesis. PLoS Genet. 2014;10:e1003954. doi: 10.1371/journal.pgen.1003954. PubMed DOI PMC

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

Vieten A., Sauer M., Brewer P.B., Friml J. Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci. 2007;12:160–168. doi: 10.1016/j.tplants.2007.03.006. PubMed DOI

Křeček P., Skůpa P., Libus J., Naramoto S., Tejos R., Friml J., Zažímalová E. The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol. 2009;10:249. doi: 10.1186/gb-2009-10-12-249. PubMed DOI PMC

Petrášek J., Mravec J., Bouchard R., Blakeslee J.J., Abas M., Seifertová D., Wisniewska J., Tadele Z., Kubeš M., Covanová 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

Wisniewska J., Xu J., Seifertová D., Brewer P.B., Růžička K., Blilou I., Rouquié D., Benková E., Scheres B., Friml J. Polar PIN localization directs auxin flow in plants. Science. 2006;312:883. doi: 10.1126/science.1121356. PubMed DOI

Mravec J., Skůpa P., Bailly A., Hoyerová K., Křeček P., Bielach A., Petrášek J., Zhang J., Gaykova V., Stierhof Y.-D., et al. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature. 2009;459:1136–1140. doi: 10.1038/nature08066. PubMed DOI

Dal Bosco C., Dovzhenko A., Palme K. Intracellular auxin transport in pollen. Plant Signal. Behav. 2012;7:1504–1505. doi: 10.4161/psb.21953. PubMed DOI PMC

Bender R.L., Fekete M.L., Klinkenberg P.M., Hampton M., Bauer B., Malecha M., Lindgren K., Maki J., Perera M.A.D., Nikolau B.J., et al. PIN6 is required for nectary auxin response and short stamen development. Plant J. 2013;74:893–904. doi: 10.1111/tpj.12184. PubMed DOI

Sawchuk M.G., Edgar A., Scarpella E. Patterning of leaf vein networks by convergent auxin transport pathways. PLoS Genet. 2013;9:e1003294. doi: 10.1371/journal.pgen.1003294. PubMed DOI PMC

Ganguly A., Lee S.H., Cho M., Lee O.R., Yoo H., Cho H.-T. Differential Auxin-Transporting Activities of PIN-FORMED Proteins in Arabidopsis Root Hair Cells. Plant Physiol. 2010;153:1046–1061. doi: 10.1104/pp.110.156505. 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

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

Kleine-Vehn J., Dhonukshe P., Sauer M., Brewer P.B., Wiśniewska J., Paciorek T., Benková E., Friml J. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol. 2008;18:526–531. doi: 10.1016/j.cub.2008.03.021. PubMed DOI

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

Dudler R., Hertig C. Structure of an mdr-like gene from Arabidopsis thaliana. Evolutionary implications. J. Biol. Chem. 1992;267:5882–5888. PubMed

Sidler M., Hassa P., Hasan S., Ringli C., Dudler R. Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. Plant Cell. 1998;10:1623–1636. doi: 10.1105/tpc.10.10.1623. PubMed DOI PMC

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

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

Noh B., Murphy A.S., Spalding E.P. Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell. 2001;13:2441–2454. doi: 10.1105/tpc.13.11.2441. PubMed DOI PMC

Blakeslee J.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

Bandyopadhyay A., Blakeslee J.J., Lee O.R., Mravec J., Sauer M., Titapiwatanakun B., Makam S.N., Bouchard R., Geisler M., Martinoia E., et al. Interactions of PIN and PGP auxin transport mechanisms. Biochem. Soc. Trans. 2007;35:137–141. doi: 10.1042/BST0350137. PubMed DOI

Geisler M., Kolukisaoglu H.U., Bouchard R., Billion K., Berger J., Saal B., Frangne N., Koncz-Kalman Z., Koncz C., Dudler R., et al. TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol. Biol. Cell. 2003;14:4238–4249. doi: 10.1091/mbc.e02-10-0698. PubMed DOI PMC

Bailly A., Sovero V., Vincenzetti V., Santelia D., Bartnik D., Koenig B.W., Mancuso S., Martinoia E., Geisler M. Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J. Biol. Chem. 2008;283:21817–21826. doi: 10.1074/jbc.M709655200. PubMed DOI

Middleton A.M., Dal Bosco C., Chlap P., Bensch R., Harz H., Ren F., Bergmann S., Wend S., Weber W., Hayashi K.-I., et al. Data-driven modeling of intracellular auxin fluxes indicates a dominant role of the ER in controlling nuclear auxin uptake. Cell Rep. 2018;22:3044–3057. doi: 10.1016/j.celrep.2018.02.074. PubMed DOI

Miller C.O., Skoog F., Okumura F.S., Von Saltza M.H., Strong F.M. Structure and synthesis of kinetin. J. Am. Chem. Soc. 1955;77:2662–2663. doi: 10.1021/ja01614a108. DOI

Miller C.O., Skoog F., Von Saltza M.H., Strong F.M. Kinetin, a cell division factor from deoxyribonucleic acid. J. Am. Chem. Soc. 1955;77:1392. doi: 10.1021/ja01610a105. DOI

Horgan R., Hewett E.W., Purse J., Wareing P.F. A new cytokinin from Populus x robusta. Tetrahedron Lett. 1973:2827–2828. doi: 10.1016/S0040-4039(01)96062-9. DOI

Horgan R., Hewett E.W., Horgan J.M., Purse J., Wareing P.F. A new cytokinin from Populus x robusta. Phytochemistry. 1975;14:1005–1008. doi: 10.1016/0031-9422(75)85176-4. DOI

Strnad M. The aromatic cytokinins. Physiol. Plant. 1997;101:674–688. doi: 10.1111/j.1399-3054.1997.tb01052.x. DOI

Persson B.C., Esberg B., Olafsson O., Björk G.R. Synthesis and function of isopentenyl adenosine derivatives in tRNA. Biochimie. 1994;76:1152–1160. doi: 10.1016/0300-9084(94)90044-2. PubMed DOI

Davies P.J. In: Plant Hormones: Biosynthesis, Signal Transduction, Action! 3rd ed. Davies P.J., editor. Kluwer Academic Publishers; Dordrecht, The Netherlands: 2010.

Cortleven A., Schmülling T. Regulation of chloroplast development and function by cytokinin. J. Exp. Bot. 2015;66:4999–5013. doi: 10.1093/jxb/erv132. PubMed DOI

Armengot L., Marquès-Bueno M.M., Jaillais Y. Regulation of polar auxin transport by protein and lipid kinases. J. Exp. Bot. 2016;67:4015–4037. doi: 10.1093/jxb/erw216. PubMed DOI PMC

Zürcher E., Müller B. Cytokinin Synthesis, Signaling, and Function-Advances and New Insights. Volume 324. Elsevier; Amsterdam, The Netherlands: 2016. PubMed

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

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

Takei K., Sakakibara H., Sugiyama T. Identification of Genes Encoding Adenylate Isopentenyltransferase, a Cytokinin Biosynthesis Enzyme, in Arabidopsis thaliana. J. Biol. Chem. 2001;276:26405–26410. doi: 10.1074/jbc.M102130200. PubMed DOI

Miyawaki K., Tarkowski P., Matsumoto-Kitano M., Kato T., Sato S., Tarkowská D., Tabata S., Sandberg G., Kakimoto T. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl. Acad. Sci. USA. 2006;103:16598–16603. doi: 10.1073/pnas.0603522103. PubMed DOI PMC

Kasahara H., Takei K., Ueda N., Hishiyama S., Yamaya T., Kamiya Y., Yamaguchi S., Sakakibara H. Distinct Isoprenoid Origins of cis- and trans-Zeatin Biosyntheses in Arabidopsis. J. Biol. Chem. 2004;279:14049–14054. doi: 10.1074/jbc.M314195200. PubMed DOI

Galichet A., Hoyerová K., Kamínek M., Gruissem W. Farnesylation directs AtIPT3 subcellular localization and modulates cytokinin biosynthesis in Arabidopsis. Plant Physiol. 2008;146:1155–1164. doi: 10.1104/pp.107.107425. PubMed DOI PMC

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

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

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

Jin S.-H., Ma X.-M., Kojima M., Sakakibara H., Wang Y.W., Hou B.-K. Overexpression of glucosyltransferase UGT85A1 influences trans-zeatin homeostasis and trans-zeatin responses likely through O-glucosylation. Planta. 2013;237:991–999. doi: 10.1007/s00425-012-1818-4. PubMed DOI

Šmehilová M., Dobrůšková J., Novák O., Takáč T., Galuszka P. Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance. Front. Plant Sci. 2016;7:1264. doi: 10.3389/fpls.2016.01264. PubMed DOI PMC

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

Moffatt B., Pethe C., Laloue M. Metabolism of Benzyladenine is Impaired in a Mutant of Arabidopsis thaliana Lacking Adenine Phosphoribosyltransferase Activity1. Plant Physiol. 1991;95:900–908. doi: 10.1104/pp.95.3.900. PubMed DOI PMC

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

Zhang X., Chen Y., Lin X., Hong X., Zhu Y., Li W., He W., An F., Guo H. Adenine phosphoribosyl transferase 1 is a key enzyme catalyzing cytokinin conversion from nucleobases to nucleotides in Arabidopsis. Mol. Plant. 2013;6:1661–1672. doi: 10.1093/mp/sst071. PubMed DOI

Mok D.W., Mok M.C. Cytokinin metabolism and action. Annu. Rev. Plant Physiol. 2001;52:89–118. doi: 10.1146/annurev.arplant.52.1.89. PubMed DOI

Pačes V., Werstiuk E., Hall R.H. Conversion of N-(Delta-Isopentenyl)adenosine to adenosine by enzyme activity in tobacco tissue. Plant Physiol. 1971;48:775–778. doi: 10.1104/pp.48.6.775. PubMed DOI PMC

Werner T., Köllmer I., Bartrina y Manns I., Holst K., Schmülling T. New insights into the biology of cytokinin degradation. Plant Biol. 2006;8:371–381. doi: 10.1055/s-2006-923928. PubMed DOI

Werner T., Motyka V., Laucou V., Smets R., Van Onckelen H.A., Schmülling T. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell. 2003;15:2532–2550. doi: 10.1105/tpc.014928. PubMed DOI PMC

Schmülling T., Werner T., Riefler M., Krupková E., Bartrina y Manns I. Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J. Plant Res. 2003;116:241–252. doi: 10.1007/s10265-003-0096-4. PubMed DOI

Niemann M.C.E., Weber H., Hluska T., Leonte G., Anderson S.M., Novák O., Senes A., Werner T. The cytokinin oxidase/dehydrogenase CKX1 is a membrane-bound protein requiring homooligomerization in the endoplasmic reticulum for its cellular activity. Plant Physiol. 2018 doi: 10.1104/pp.17.00925. PubMed DOI PMC

Köllmer I., Novák O., Strnad M., Schmülling T., Werner T. Overexpression of the cytosolic cytokinin oxidase/dehydrogenase (CKX7) from Arabidopsis causes specific changes in root growth and xylem differentiation. Plant J. 2014;78:359–371. doi: 10.1111/tpj.12477. PubMed DOI

Galuszka P., Popelková H., Werner T., Frébortová J., Pospíšilová H., Mik V., Köllmer I., Schmülling T., Frébort I. Biochemical Characterization of Cytokinin Oxidases/Dehydrogenases from Arabidopsis thaliana Expressed in Nicotiana tabacum L. J. Plant Growth Regul. 2007;26:255–267. doi: 10.1007/s00344-007-9008-5. DOI

Kowalska M., Galuszka P., Frébortová J., Šebela M., Béreš T., Hluska T., Šmehilová M., Bilyeu K.D., Frébort I. Vacuolar and cytosolic cytokinin dehydrogenases of Arabidopsis thaliana: Heterologous expression, purification and properties. Phytochemistry. 2010;71:1970–1978. doi: 10.1016/j.phytochem.2010.08.013. PubMed DOI

Corbesier L., Prinsen E., Jacqmard A., Lejeune P., Van Onckelen H.A., Périlleux C., Bernier G. Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition. J. Exp. Bot. 2003;54:2511–2517. doi: 10.1093/jxb/erg276. PubMed 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

Kudo T., Kiba T., Sakakibara H. Metabolism and long-distance translocation of cytokinins. J. Integr. Plant Biol. 2010;52:53–60. doi: 10.1111/j.1744-7909.2010.00898.x. 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

Gillissen B., Bürkle L., André B., Kühn C., Rentsch D., Brandl B., Frommer W.B. A new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis. Plant Cell. 2000;12:291–300. doi: 10.1105/tpc.12.2.291. PubMed DOI PMC

Wormit A., Traub M., Flörchinger M., Neuhaus H.E., Möhlmann T. Characterization of three novel members of the Arabidopsis thaliana equilibrative nucleoside transporter (ENT) family. Biochem. J. 2004;383:19–26. doi: 10.1042/BJ20040389. PubMed DOI PMC

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., Novák 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

Kiran N.S., Polanská L., Fohlerová R., Mazura P., Válková M., Šmeral M., Zouhar J., Malbeck J., Dobrev P.I., Macháčková I., et al. Ectopic over-expression of the maize β-glucosidase Zm-p60.1 perturbs cytokinin homeostasis in transgenic tobacco. J. Exp. Bot. 2006;57:985–996. doi: 10.1093/jxb/erj084. PubMed DOI

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

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

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. doi: 10.1071/FP16292. PubMed DOI

Kim H.J., Ryu H., Hong S.H., Woo H.R., Lim P.O., Lee I.C., Sheen J., Nam H.-G., Hwang I. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2006;103:814–819. doi: 10.1073/pnas.0505150103. PubMed DOI PMC

Caesar K., Thamm A.M.K., Witthöft J., Elgass K., Huppenberger P., Grefen C., Horak J., Harter K. Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. J. Exp. Bot. 2011;62:5571–5580. doi: 10.1093/jxb/err238. PubMed DOI PMC

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

Punwani J.A., Hutchison C.E., Schaller G.E., Kieber J.J. The subcellular distribution of the Arabidopsis histidine phosphotransfer proteins is independent of cytokinin signaling. Plant J. 2010;62:473–482. doi: 10.1111/j.1365-313X.2010.04165.x. PubMed DOI

Mähönen A.P., Bishopp A., Higuchi M., Nieminen K.M., Kinoshita K., Törmäkangas K., Ikeda Y., Oka A., Kakimoto T., Helariutta Y. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science. 2006;311:94–98. doi: 10.1126/science.1118875. PubMed DOI

Suzuki T., Sakurai K., Imamura A., Nakamura A., Ueguchi C., Mizuno T. Compilation and characterization of histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in plants: AHP signal transducers of Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 2000;64:2486–2489. doi: 10.1271/bbb.64.2486. PubMed DOI

Kiba T., Taniguchi M., Imamura A., Ueguchi C., Mizuno T., Sugiyama T. Differential expression of genes for response regulators in response to cytokinins and nitrate in Arabidopsis thaliana. Plant Cell Physiol. 1999;40:767–771. doi: 10.1093/oxfordjournals.pcp.a029604. PubMed DOI

Mason M.G., Li J., Mathews D.E., Kieber J.J., Schaller G.E. Type-B response regulators display overlapping expression patterns in Arabidopsis. Plant Physiol. 2004;135:927–937. doi: 10.1104/pp.103.038109. PubMed DOI PMC

D’Agostino Ingrid B., Deruère J., Kieber J.J. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 2000;124:1706–1717. doi: 10.1104/pp.124.4.1706. PubMed DOI PMC

Rashotte A.M., Carson S.D.B., To J.P.C., Kieber J.J. Expression profiling of cytokinin action in Arabidopsis. Plant Physiol. 2003;132:1998–2011. doi: 10.1104/pp.103.021436. PubMed DOI PMC

To J.P.C., Haberer G., Ferreira F.J., Deruère J., Mason M.G., Schaller G.E., Alonso J.M., Ecker J.R., Kieber J.J. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell. 2004;16:658–671. doi: 10.1105/tpc.018978. PubMed DOI PMC

Li J., Wang D. Cloning and in vitro expression of the cDNA encoding a putative nucleoside transporter from Arabidopsis thaliana. Plant Sci. 2000;157:23–32. doi: 10.1016/S0168-9452(00)00261-2. PubMed DOI

Möhlmann T., Mezher Z., Schwerdtfeger G., Neuhaus H.E. Characterisation of a concentrative type of adenosine transporter from Arabidopsis thaliana (ENT1,At) FEBS Lett. 2001;509:370–374. doi: 10.1016/S0014-5793(01)03195-7. PubMed DOI

Li G., Liu K., Baldwin S.A., Wang D. Equilibrative nucleoside transporters of Arabidopsis thaliana. cDNA cloning, expression pattern, and analysis of transport activities. J. Biol. Chem. 2003;278:35732–35742. doi: 10.1074/jbc.M304768200. PubMed DOI

Jaquinod M., Villiers F., Kieffer-Jaquinod S., Hugouvieux V., Bruley C., Garin J., Bourguignon J. A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell. Proteom. 2007;6:394–412. doi: 10.1074/mcp.M600250-MCP200. PubMed DOI PMC

Petersson S.V., Johansson A.I., Kowalczyk M., Makoveychuk A., Wang J.Y., Moritz T., Grebe M., Benfey P.N., Sandberg G., Ljung K. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell. 2009;21:1659–1668. doi: 10.1105/tpc.109.066480. PubMed DOI PMC

Antoniadi I., Plačková L., Simonovik B., Doležal K., Turnbull C., Ljung K., Novák O. Cell-type-specific cytokinin distribution within the Arabidopsis primary root apex. Plant Cell. 2015;27:1955–1967. doi: 10.1105/tpc.15.00176. PubMed DOI PMC

Hayashi K., Nakamura S., Fukunaga S., Nishimura T., Jenness M.K., Murphy A.S., Motose H., Nozaki H., Furutani M., Aoyama T. Auxin transport sites are visualized in planta using fluorescent auxin analogs. Proc. Natl. Acad. Sci. USA. 2014;111:11557–11562. doi: 10.1073/pnas.1408960111. PubMed DOI PMC

Bieleszová K., Pařízková B., Kubeš M., Husičková A., Kubala M., Ma Q., Sedlářová M., Robert S., Doležal K., Strnad M., et al. New fluorescently labeled auxins exhibit promising anti-auxin activity. New Biotechnol. 2018 doi: 10.1016/j.nbt.2018.06.003. PubMed DOI

Kubiasová K., Mik V., Nisler J., Hönig M., Husičková A., Spíchal L., Pěkná Z., Šamajová O., Doležal K., Plíhal O., et al. Design, synthesis and perception of fluorescently labeled isoprenoid cytokinins. Phytochemistry. 2018;150:1–11. doi: 10.1016/j.phytochem.2018.02.015. PubMed DOI

Hošek P., Kubeš M., Laňková M., Dobrev P.I., Klíma P., Kohoutová M., Petrášek J., Hoyerová K., Jiřina M., Zažímalová E. Auxin transport at cellular level: New insights supported by mathematical modelling. J. Exp. Bot. 2012;63:3815–3827. doi: 10.1093/jxb/ers074. PubMed DOI PMC

Dynamic changes of endogenous phytohormones and carbohydrates during spontaneous morphogenesis of Centaurium erythraea Rafn

Auxin Metabolite Profiling in Isolated and Intact Plant Nuclei

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

Differential Subcellular Distribution of Cytokinins: How Does Membrane Transport Fit into the Big Picture?

A Stimulatory Role for Cytokinin in the Arbuscular Mycorrhizal Symbiosis of Pea