Advertisement

Planta

, 251:1 | Cite as

Characterization of five CHASE-containing histidine kinase receptors from Populus × canadensis cv. Robusta sensing isoprenoid and aromatic cytokinins

  • Pavel Jaworek
  • Petr Tarkowski
  • Tomáš Hluska
  • Štěpán Kouřil
  • Ondřej Vrobel
  • Jaroslav Nisler
  • David KopečnýEmail author
Original Article
  • 38 Downloads

Abstract

Main conclusion

Five poplar CHASE-containing histidine kinase receptors bind cytokinins and display kinase activities. Both endogenous isoprenoid and aromatic cytokinins bind to the receptors in live cell assays.

Abstract

Cytokinins are phytohormones that play key roles in various developmental processes in plants. The poplar species Populus × canadensis, cv. Robusta, is the first organism found to contain aromatic cytokinins. Here, we report the functional characterization of five CHASE-containing histidine kinases from P. × canadensis: PcHK2, PcHK3a, PcHK3b, PcHK4a and PcHK4b. A qPCR analysis revealed high transcript levels of all PcHKs other than PcHK4b across multiple poplar organs. The ligand specificity was determined using a live cell Escherichia coli assay and we provide evidence based on UHPLC-MS/MS data that ribosides can be true ligands. PcHK2 exhibited higher sensitivity to iP-type cytokinins than the other receptors, while PcHK3a and PcHK3b bound these cytokinins much more weakly, because they possess two isoleucine residues that clash with the cytokinin base and destabilize its binding. All receptors display kinase activity but their activation ratios in the presence/absence of cytokinin differ significantly. PcHK4a displays over 400-fold higher kinase activity in the presence of cytokinin, suggesting involvement in strong responses to changes in cytokinin levels. trans-Zeatin was both the most abundant cytokinin in poplar and that with the highest variation in abundance, which is consistent with its strong binding to all five HKs and activation of cytokinin signaling via A-type response regulators. The aromatic cytokinins’ biological significance remains unclear, their levels vary diurnally, seasonally, and annually. PcHK3 and PcHK4 display the strongest binding at pH 7.5 and 5.5, respectively, in line with their putative membrane localization in the endoplasmic reticulum and plasma membrane.

Keywords

Aromatic cytokinin Histidine kinase Hormone Isoprenoid cytokinin Poplar Topolin 

Abbreviations

3FMTDZ

1-[1,2,3]thiadiazol-5-yl-3-(3-trifluoromethoxy-phenyl)urea

BAP

N6-benzyladenine

cZ

N6-(cis-4-hydroxy-3-methyl-2-buten-1-yl)adenine, i.e. cis-zeatin

iP

N6-(2-isopentenyl)adenine

iPR

N6-(2-isopentenyl)adenosine

mT

meta-topolin

HETDZ

1-[2-(2-hydroxy-ethyl)phenyl]-3-(1,2,3-thiadiazol-5-yl)urea

HK

Histidine kinase

oT

ortho-Topolin

RR

Response regulators

TDZ

N-(1,2,3-thidiazol-5-yl)-N´-phenylurea, i.e. thidiazuron

tZ

trans-Zeatin

tZR

Zeatin riboside

Notes

Acknowledgements

This work was supported by the grant 15-16888S from the Czech Science Foundation, institutional support MZE-RO0418 and IGA_PrF_2018_033 (Palacký University, Olomouc, CZ). DK and PT were supported also from ERDF project “Plants as a tool for sustainable global development” (No. CZ.02.1.01/0.0/0.0/16_019/0000827). We acknowledge Zuzana Pěkná and Lukáš Spíchal for their help with the live cell competitive binding assay (Palacký University, Olomouc, CZ) and prof. Peter Hedden for proofreading the manuscript. Poplar calli were derived from dormant leaf buds provided by Dr. Jana Malá from Forestry and Game Management Research Institute (Jíloviště, CZ). The pINIIIΔEH vector and E. coli strain KMI001 were kindly provided by Dr. Zalabák (Palacký University, Olomouc, CZ). The authors are grateful to Sees-editing Ltd. (UK) for editing the manuscript. Populus deltoides sequence data were produced by the US Department of Energy Joint Genome Institute http://www.jgi.doe.gov.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest with the contents of this article.

Supplementary material

425_2019_3297_MOESM1_ESM.docx (111 kb)
Supplementary material 1 (DOCX 110 kb)

References

  1. Bar M, Israeli A, Levy M et al (2016) CLAUSA is a MYB transcription factor that promotes leaf differentiation by attenuating cytokinin signaling. Plant Cell 28:1602–1615.  https://doi.org/10.1105/tpc.16.00211 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bartrina I, Jensen H, Novák O et al (2017) Gain-of-function mutants of the cytokinin receptors AHK2 and AHK3 regulate plant organ size, flowering time and plant longevity. Plant Physiol 173:1783–1797.  https://doi.org/10.1104/pp.16.01903 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beveridge CA, Murfet IC, Kerhoas L et al (1997) The shoot controls zeatin riboside export from pea roots. Evidence from the branching mutant rms4. Plant J 11:339–345.  https://doi.org/10.1046/j.1365-313X.1997.11020339.x CrossRefGoogle Scholar
  4. Caesar K, Thamm AMK, Witthöft J et al (2011) Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. J Exp Bot 62:5571–5580.  https://doi.org/10.1093/jxb/err238 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552.  https://doi.org/10.1093/oxfordjournals.molbev.a026334 CrossRefPubMedGoogle Scholar
  6. Cheng Y, Prusoff WH (1973) Relationship between the inhibition constant (KI) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 22:3099–3108CrossRefGoogle Scholar
  7. Choi J, Lee J, Kim K et al (2012) Functional identification of OsHk6 as a homotypic cytokinin receptor in rice with preferential affinity for iP. Plant Cell Physiol 53:1334–1343.  https://doi.org/10.1093/pcp/pcs079 CrossRefPubMedGoogle Scholar
  8. Corbesier L, Prinsen E, Jacqmard A et al (2003) Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition. J Exp Bot 54:2511–2517.  https://doi.org/10.1093/jxb/erg276 CrossRefPubMedGoogle Scholar
  9. D’Agostino IB, Deruère J, Kieber JJ (2000) Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol 124:1706–1717.  https://doi.org/10.1104/pp.124.4.1706 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Daudu D, Allion E, Liesecke F et al (2017) CHASE-containing histidine kinase receptors in apple tree: from a common receptor structure to divergent cytokinin binding properties and specific functions. Front Plant Sci 8:1614.  https://doi.org/10.3389/fpls.2017.01614 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dobránszki J, Mendler-Drienyovszki N (2014) Cytokinin-induced changes in the chlorophyll content and fluorescence of in vitro apple leaves. J Plant Physiol 171:1472–1478.  https://doi.org/10.1016/j.jplph.2014.06.015 CrossRefPubMedGoogle Scholar
  12. Dortay H, Mehnert N, Bürkle L et al (2006) Analysis of protein interactions within the cytokinin-signaling pathway of Arabidopsis thaliana. FEBS J 273:4631–4644.  https://doi.org/10.1111/j.1742-4658.2006.05467.x CrossRefPubMedGoogle Scholar
  13. Du L, Jiao F, Chu J et al (2007) The two-component signal system in rice (Oryza sativa L.): a genome-wide study of cytokinin signal perception and transduction. Genomics 89:697–707.  https://doi.org/10.1016/j.ygeno.2007.02.001 CrossRefPubMedGoogle Scholar
  14. Edlund E, Novak O, Karady M et al (2017) Contrasting patterns of cytokinins between years in senescing aspen leaves. Plant, Cell Environ 40:622–634.  https://doi.org/10.1111/pce.12899 CrossRefGoogle Scholar
  15. Guindon S, Dufayard J-F, Lefort V et al (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321.  https://doi.org/10.1093/sysbio/syq010 CrossRefPubMedGoogle Scholar
  16. Hewett EW, Wareing PF (1973) Cytokinins in Populus x robusta (schneid): light effects on endogenous levels. Planta 114:119–129.  https://doi.org/10.1007/BF00387470 CrossRefPubMedGoogle Scholar
  17. Heyl A, Wulfetange K, Pils B et al (2007) Evolutionary proteomics identifies amino acids essential for ligand-binding of the cytokinin receptor CHASE domain. BMC Evol Biol 7:62.  https://doi.org/10.1186/1471-2148-7-62 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Higuchi M, Pischke MS, Mähönen AP et al (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci 101:8821–8826.  https://doi.org/10.1073/pnas.0402887101 CrossRefPubMedGoogle Scholar
  19. Hirose N, Takei K, Kuroha T et al (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59:75–83.  https://doi.org/10.1093/jxb/erm157 CrossRefPubMedGoogle Scholar
  20. Horgan R, Hewett EW, Purse JG, Wareing PF (1973) A new cytokinin from Populus robusta. Tetrahedron Lett 14:2827–2828.  https://doi.org/10.1016/S0040-4039(01)96062-9 CrossRefGoogle Scholar
  21. Hothorn M, Dabi T, Chory J (2011) Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat Chem Biol 7:766–768.  https://doi.org/10.1038/nchembio.667 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Huang X, Miller W (1991) A time-efficient, linear-space local similarity algorithm. Adv Appl Math 12:337–357.  https://doi.org/10.1016/0196-8858(91)90017-D CrossRefGoogle Scholar
  23. Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383–389.  https://doi.org/10.1038/35096500 CrossRefPubMedGoogle Scholar
  24. Immanen J, Nieminen K, Silva HD et al (2013) Characterization of cytokinin signaling and homeostasis gene families in two hardwood tree species: Populus trichocarpa and Prunus persica. BMC Genom 14:885.  https://doi.org/10.1186/1471-2164-14-885 CrossRefGoogle Scholar
  25. Inoue T, Higuchi M, Hashimoto Y et al (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063.  https://doi.org/10.1038/35059117 CrossRefPubMedGoogle Scholar
  26. Jaworek P, Kopečný D, Zalabák D et al (2019) Occurrence and biosynthesis of cytokinins in poplar. Planta 250:229–244.  https://doi.org/10.1007/s00425-019-03152-z CrossRefPubMedGoogle Scholar
  27. Kieber JJ, Schaller GE (2014) Cytokinins. Arab Book.  https://doi.org/10.1199/tab.0168 CrossRefGoogle Scholar
  28. Kim HJ, Ryu H, Hong SH et al (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci 103:814–819.  https://doi.org/10.1073/pnas.0505150103 CrossRefPubMedGoogle Scholar
  29. Kopečná M, Blaschke H, Kopečný D et al (2013) Structure and function of nucleoside hydrolases from Physcomitrella patens and maize catalyzing the hydrolysis of purine, pyrimidine, and cytokinin ribosides. Plant Physiol 163:1568–1583.  https://doi.org/10.1104/pp.113.228775 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kopečný D, Briozzo P, Popelková H et al (2010) Phenyl- and benzylurea cytokinins as competitive inhibitors of cytokinin oxidase/dehydrogenase: a structural study. Biochimie 92:1052–1062.  https://doi.org/10.1016/j.biochi.2010.05.006 CrossRefPubMedGoogle Scholar
  31. Kopečný D, Končitíková R, Popelka H et al (2016) Kinetic and structural investigation of the cytokinin oxidase/dehydrogenase active site. FEBS J 283:361–377.  https://doi.org/10.1111/febs.13581 CrossRefPubMedGoogle Scholar
  32. Kubiasová K, Mik V, Nisler J et al (2018) Design, synthesis and perception of fluorescently labeled isoprenoid cytokinins. Phytochemistry 150:1–11.  https://doi.org/10.1016/j.phytochem.2018.02.015 CrossRefPubMedGoogle Scholar
  33. Kuderová A, Gallová L, Kuricová K et al (2015) Identification of AHK2- and AHK3-like cytokinin receptors in Brassica napus reveals two subfamilies of AHK2 orthologues. J Exp Bot 66:339–353.  https://doi.org/10.1093/jxb/eru422 CrossRefPubMedGoogle Scholar
  34. Lomin SN, Yonekura-Sakakibara K, Romanov GA, Sakakibara H (2011) Ligand-binding properties and subcellular localization of maize cytokinin receptors. J Exp Bot 62:5149–5159.  https://doi.org/10.1093/jxb/err220 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lomin SN, Krivosheev DM, Steklov MY et al (2015) Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands. J Exp Bot 66:1851–1863.  https://doi.org/10.1093/jxb/eru522 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lomin SN, Myakushina YA, Kolachevskaya OO et al (2018) Cytokinin perception in potato: new features of canonical players. J Exp Bot 69:3839–3853.  https://doi.org/10.1093/jxb/ery199 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mähönen AP, Bonke M, Kauppinen L et al (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14:2938–2943CrossRefGoogle Scholar
  38. Malito E, Coda A, Bilyeu KD, Fraaije MW, Mattevi A (2004) Structures of Michaelis and product complexes of plant cytokinin dehydrogenase: implications for flavoenzyme catalysis. J Mol Biol 341:1237–1249.  https://doi.org/10.1016/j.jmb.2004.06.083 CrossRefPubMedGoogle Scholar
  39. Martinière A, Bassil E, Jublanc E et al (2013) In vivo intracellular pH measurements in tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system. Plant Cell 25:4028–4043.  https://doi.org/10.1105/tpc.113.116897 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Miwa K, Ishikawa K, Terada K et al (2007) Identification of amino acid substitutions that render the Arabidopsis cytokinin receptor histidine kinase AHK4 constitutively active. Plant Cell Physiol 48:1809–1814.  https://doi.org/10.1093/pcp/pcm145 CrossRefPubMedGoogle Scholar
  41. Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118.  https://doi.org/10.1146/annurev.arplant.52.1.89 CrossRefPubMedGoogle Scholar
  42. Mok MC, Mok DWS, Armstrong DJ et al (1982) Cytokinin activity of N-phenyl-N′-1,2,3-thiadiazol-5-ylurea (thidiazuron). Phytochemistry 21:1509–1511.  https://doi.org/10.1016/S0031-9422(82)85007-3 CrossRefGoogle Scholar
  43. Müller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094–1097.  https://doi.org/10.1038/nature06943 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nishimura C, Ohashi Y, Sato S et al (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377.  https://doi.org/10.1105/tpc.021477 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Nisler J, Kopečný D, Končitíková R et al (2016) Novel thidiazuron-derived inhibitors of cytokinin oxidase/dehydrogenase. Plant Mol Biol 92:235–248.  https://doi.org/10.1007/s11103-016-0509-0 CrossRefPubMedGoogle Scholar
  46. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217.  https://doi.org/10.1006/jmbi.2000.4042 CrossRefGoogle Scholar
  47. Novák O, Hauserová E, Amakorová P et al (2008) Cytokinin profiling in plant tissues using ultra-performance liquid chromatography–electrospray tandem mass spectrometry. Phytochemistry 69:2214–2224.  https://doi.org/10.1016/j.phytochem.2008.04.022 CrossRefPubMedGoogle Scholar
  48. Pils B, Heyl A (2009) Unraveling the evolution of cytokinin signaling. Plant Physiol 151:782–791.  https://doi.org/10.1104/pp.109.139188 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ramírez-Carvajal GA, Morse AM, Davis JM (2008) Transcript profiles of the cytokinin response regulator gene family in Populus imply diverse roles in plant development. New Phytol 177:77–89.  https://doi.org/10.1111/j.1469-8137.2007.02240.x CrossRefPubMedGoogle Scholar
  50. Rashotte AM, Carson SD, To JP, Kieber JJ (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol 132:1998–2011.  https://doi.org/10.1104/pp.103.021436 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Rittenberg D, Foster GL (1940) A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. J Biol Chem 133:737–744Google Scholar
  53. Romanov GA, Spíchal L, Lomin SN et al (2005) A live cell hormone-binding assay on transgenic bacteria expressing a eukaryotic receptor protein. Anal Biochem 347:129–134.  https://doi.org/10.1016/j.ab.2005.09.012 CrossRefPubMedGoogle Scholar
  54. 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 CrossRefPubMedGoogle Scholar
  55. Scatchard G (1949) The attractions of proteins for small molecules and ions. Ann NY Acad Sci 51:660–672.  https://doi.org/10.1111/j.1749-6632.1949.tb27297.x CrossRefGoogle Scholar
  56. Schoor S, Farrow S, Blaschke H et al (2011) Adenosine kinase contributes to cytokinin interconversion in Arabidopsis. Plant Physiol 157:659–672.  https://doi.org/10.1104/pp.111.181560 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sorrentino G, Haworth M, Wahbi S et al (2016) Abscisic acid induces rapid reductions in mesophyll conductance to carbon dioxide. PLoS One 11:e0148554.  https://doi.org/10.1371/journal.pone.0148554 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Spíchal L (2011) Bacterial assay to study plant sensor histidine kinases. In: Dissmeyer N, Schnittger A (eds) Plant kinases. Humana Press, Totowa, pp 139–147.  https://doi.org/10.1007/978-1-61779-264-9 Google Scholar
  59. Spíchal L, Rakova NY, Riefler M et al (2004) Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant Cell Physiol 45:1299–1305.  https://doi.org/10.1093/pcp/pch132 CrossRefPubMedGoogle Scholar
  60. Stolz A, Riefler M, Lomin SN et al (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 CrossRefPubMedGoogle Scholar
  61. Strnad M (1997) The aromatic cytokinins. Physiol Plant 101:674–688.  https://doi.org/10.1111/j.1399-3054.1997.tb01052.x CrossRefGoogle Scholar
  62. Strnad M, Peters W, Beck E, Kamínek M (1992) Immunodetection and identification of N6-(o-hydroxybenzylamino)purine as a naturally cccurring cytokinin in Populus x canadensis Moench cv Robusta leaves. Plant Physiol 99:74–80CrossRefGoogle Scholar
  63. Strnad M, Peters W, Hanuš J, Beck E (1994) Ortho-topolin-9-glucoside, an aromatic cytokinin from Populus x canadensis cv Robusta leaves. Phytochemistry 37:1059–1062.  https://doi.org/10.1016/S0031-9422(00)89528-X CrossRefGoogle Scholar
  64. Strnad M, Hanus J, Vanek T et al (1997) Meta-topolin, a highly active aromatic cytokinin from poplar leaves (Populus x canadensis moench., cv. Robusta). Phytochemistry 45:213–218.  https://doi.org/10.1016/S0031-9422(96)00816-3 CrossRefGoogle Scholar
  65. Suzuki T, Miwa K, Ishikawa K et al (2001) The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol 42:107–113.  https://doi.org/10.1093/pcp/pce037 CrossRefPubMedGoogle Scholar
  66. Takeda S, Fujisawa Y, Matsubara M et al (2001) A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC → YojN → RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol Microbiol 40:440–450.  https://doi.org/10.1046/j.1365-2958.2001.02393.x CrossRefPubMedGoogle Scholar
  67. Tirichine L, Sandal N, Madsen LH et al (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107.  https://doi.org/10.1126/science.1132397 CrossRefPubMedGoogle Scholar
  68. To JP, Haberer G, Ferreira FJ et al (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 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Tran LSP, Urao T, Qin F et al (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623–20628.  https://doi.org/10.1073/pnas.0706547105 CrossRefPubMedGoogle Scholar
  70. Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604.  https://doi.org/10.1126/science.1128691 CrossRefGoogle Scholar
  71. Ueguchi C, Koizumi H, Suzuki T, Mizuno T (2001) Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol 42:231–235.  https://doi.org/10.1093/pcp/pce015 CrossRefPubMedGoogle Scholar
  72. Wang F-F, Cheng S-T, Wu Y et al (2017) A bacterial receptor PcrK senses the plant hormone cytokinin to promote adaptation to oxidative stress. Cell Rep 21:2940–2951.  https://doi.org/10.1016/j.celrep.2017.11.017 CrossRefPubMedGoogle Scholar
  73. Waterhouse A, Bertoni M, Bienert S et al (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucl Acids Res 46:W296–W303.  https://doi.org/10.1093/nar/gky427 CrossRefPubMedGoogle Scholar
  74. Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538.  https://doi.org/10.1016/j.pbi.2009.07.002 CrossRefPubMedGoogle Scholar
  75. Wulfetange K, Lomin SN, Romanov GA et al (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 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Yamada H, Suzuki T, Terada K et al (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–1023CrossRefGoogle Scholar
  77. Yonekura-Sakakibara K, Kojima M, Yamaya T, Sakakibara H (2004) Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cis-zeatin. Plant Physiol 134:1654–1661.  https://doi.org/10.1104/pp.103.037176 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Pavel Jaworek
    • 1
    • 2
  • Petr Tarkowski
    • 1
    • 3
  • Tomáš Hluska
    • 3
  • Štěpán Kouřil
    • 1
  • Ondřej Vrobel
    • 1
    • 3
  • Jaroslav Nisler
    • 4
  • David Kopečný
    • 2
    Email author
  1. 1.Department of Phytochemistry, Faculty of Science, Centre of the Region Haná for Biotechnological and Agricultural ResearchPalacký University OlomoucOlomoucCzech Republic
  2. 2.Department of Protein Biochemistry and Proteomics, Faculty of Science, Centre of the Region Haná for Biotechnological and Agricultural ResearchPalacký University OlomoucOlomoucCzech Republic
  3. 3.Department of Genetic Resources for Vegetables, Medicinal and Special Plants, Centre of the Region Haná for Biotechnological and Agricultural ResearchCrop Research InstituteOlomoucCzech Republic
  4. 4.Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental BotanyAS CR & Palacký UniversityOlomoucCzech Republic

Personalised recommendations