Plant Cell Reports

, Volume 32, Issue 6, pp 781–793 | Cite as

Structural basis for cytokinin receptor signaling: an evolutionary approach

  • Mikhail Yu. Steklov
  • Sergey N. Lomin
  • Dmitry I. Osolodkin
  • Georgy A. Romanov
Review

Abstract

Cytokinins are ubiquitous plant hormones; their signal is perceived by sensor histidine kinases—cytokinin receptors. This review focuses on recent advances on cytokinin receptor structure, in particular sensing module and adjacent domains which play an important role in hormone recognition, signal transduction and receptor subcellular localization. Principles of cytokinin binding site organization and point mutations affecting signaling are discussed. To date, more than 100 putative cytokinin receptor genes from different plant species were revealed due to the total genome sequencing. This allowed us to employ an evolutionary and bioinformatics approaches to clarify some new aspects of receptor structure and function. Non-transmembrane areas adjacent to the ligand-binding CHASE domain were characterized in detail and new conserved protein motifs were recovered. Putative mechanisms for cytokinin-triggered receptor activation were suggested.

Keywords

Cytokinin Receptor CHASE domain PAS domain Transmembrane helix Consensus motifs Hormone signaling 

References

  1. Anantharaman V, Aravind L (2001) The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem Sci 26:579–582PubMedCrossRefGoogle Scholar
  2. Bishopp A, Help H, Helariutta Y (2009) Cytokinin signaling during root development. Int Rev Cell Mol Biol 276:1–48PubMedCrossRefGoogle Scholar
  3. Bond CS (2003) TopDraw: a sketchpad for protein structure topology cartoons. Bioinformatics 19:311–312. doi:10.1093/bioinformatics/19.2.311 PubMedCrossRefGoogle Scholar
  4. Brandizzi F, Frangne N, Marc-Martin S, Hawes C, Neuhaus JM, Paris N (2002) The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 4:1077–1092Google Scholar
  5. Brenner WG, Ramireddy E, Heyl A, Schmülling T (2012) Gene regulation by cytokinin in Arabidopsis. Front Plant Sci 3:8PubMedCrossRefGoogle Scholar
  6. Caesar K, Thamm AM, Witthöft J, Elgass K, Huppenberger P, Grefen C, Horak J, Harter K (2011) Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. J Exp Bot 62:5571–5580PubMedCrossRefGoogle Scholar
  7. Cheung J, Hendrickson WA (2009) Structural analysis of ligand stimulation of the histidine kinase NarX. Structure 17:190–201PubMedCrossRefGoogle Scholar
  8. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190PubMedCrossRefGoogle Scholar
  9. Falke JJ, Erbse AH (2009) The piston rises again. Structure 17:1149–1151PubMedCrossRefGoogle Scholar
  10. Grefen C, Harter K (2004) Plant two-component systems: principles, functions, complexity and cross talk. Planta 219:733–742PubMedCrossRefGoogle Scholar
  11. Gupta S, Rashotte AM (2012) Down-stream components of cytokinin signaling and the role of cytokinin throughout the plant. Plant Cell Rep 31:801–812PubMedCrossRefGoogle Scholar
  12. Haberer G, Kieber JJ (2002) Cytokinins. New insights into a classic phytohormone. Plant Physiol 128:354–362PubMedCrossRefGoogle Scholar
  13. Han Q, Jiang H, Qi X, Yu J, Wu P (2004) A CHASE domain containing protein kinase OsCRL4 represents a new AtCRE1-like gene family in rice. J Zhejiang Univ Sci 5:629–633PubMedCrossRefGoogle Scholar
  14. Henry JT, Crosson S (2011) Ligand-Binding PAS Domains in a Genomic, Cellular, and Structural Context. Annu Rev Microbiol 65:261–286PubMedCrossRefGoogle Scholar
  15. Heyl A, Schmülling T (2003) Cytokinin signal perception and transduction. Curr Opin Plant Biol 6:480–488PubMedCrossRefGoogle Scholar
  16. Heyl A, Wulfetange K, Pils B, Nielsen N, Romanov GA, Schmülling T (2007) Evolutionary proteomics identifies amino acids essential for ligand-binding of the cytokinin receptor CHASE domain. BMC Evol Biol 7:62PubMedCrossRefGoogle Scholar
  17. Heyl A, Riefler M, Romanov GA, Schmülling T (2012) Properties, functions and evolution of cytokinin receptors. Eur J Cell Biol 91:246–256PubMedCrossRefGoogle Scholar
  18. Heyl A, Brault M, Frugier F, Kuderová A, Lindner AC, Motyka V, Rashotte AM, von Schwartzenberg K, Vankova R, Schaller E (2013) Nomenclature for members of the two-component signaling pathway of plants. Plant Physiol 161:1063–1065 Google Scholar
  19. Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, Sakakibara H (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59:75–83PubMedCrossRefGoogle Scholar
  20. Hothorn M, Dabi T, Chory J (2011) Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat Chem Biol 7:766–768PubMedCrossRefGoogle Scholar
  21. Hwang I, Chen H, Sheen J (2002) Two-component signal transduction pathway in Arabidopsis. Plant Physiol 129:500–515PubMedCrossRefGoogle Scholar
  22. Kakimoto T (2003) Perception and signal transduction of cytokinins. Annu Rev Plant Biol 54:605–627Google Scholar
  23. Lomin SN, Yonekura-Sakakibara K, Romanov GA, Sakakibara H (2011) Ligand-binding properties and subcellular localization of maize cytokinin receptors. J Exp Bot 62:5149–5159PubMedCrossRefGoogle Scholar
  24. Lomin SN, Krivosheev DM, Steklov MYu, Osolodkin DI, Romanov GA (2012) Receptor properties and features of cytokinin signaling. Acta Naturae 4(3):31–45PubMedGoogle Scholar
  25. Miwa K, Ishikawa K, Terada K, Yamada H, Suzuki T, Yamashino T, Mizuno T (2007) Identification of amino acid substitutions that render the Arabidopsis cytokinin receptor histidine kinase AHK4 constitutively active. Plant Cell Physiol 48:1809–1814PubMedCrossRefGoogle Scholar
  26. Möglich A, Ayers RA, Moffat K (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17:1282–1294PubMedCrossRefGoogle Scholar
  27. Moore JO, Hendrickson WA (2009) Structural analysis of sensor domains from the TMAO-responsive histidine kinase receptor TorS. Structure 17:1195–1204PubMedCrossRefGoogle Scholar
  28. Mougel C, Zhulin IB (2001) CHASE: an extracellular sensing domain common to transmembrane receptors from prokaryotes, lower eukaryotes and plants. Trends Biochem Sci 26:582–584PubMedCrossRefGoogle Scholar
  29. Müller B, Sheen J (2007) Advances in cytokinin signaling. Science 318:68–69PubMedCrossRefGoogle Scholar
  30. Pas J, von Grotthuss M, Wyrwicz LS, Rychlewski L, Barciszewski J (2004) Structure prediction, evolution and ligand interaction of CHASE domain. FEBS Lett 576:287–290PubMedCrossRefGoogle Scholar
  31. Pils B, Heyl A (2009) Unraveling the evolution of cytokinin signaling. Plant Physiol 151:782–791PubMedCrossRefGoogle Scholar
  32. Romanov GA (2009) How do cytokinins affect the cell? Russ J Plant Physiol 56:268–290CrossRefGoogle Scholar
  33. Romanov GA (2012) Cytokinins. McGraw Hill Encyclopedia of Science & Technol 5:205–207Google Scholar
  34. 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 57:4051–4058PubMedCrossRefGoogle Scholar
  35. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449PubMedCrossRefGoogle Scholar
  36. Schaller GE, Shiu S-H, Armitage JP (2011) Two-component systems and their co-option for eukaryotic signal transduction. Curr Biol 21:R320–R330PubMedCrossRefGoogle Scholar
  37. Schneider TD, Stephens RM (1990) Sequence Logos: a new way to display consensus sequences. Nucl Acids Res. 18:6097–6100PubMedCrossRefGoogle Scholar
  38. Shi X, Rashotte AM (2012) Advances in upstream players of cytokinin phosphorelay: receptors and histidine phosphotransfer proteins. Plant Cell Rep 31:789–799PubMedCrossRefGoogle Scholar
  39. Slavny P, Little R, Salinas P, Clarke TA, Dixon R (2010) Quaternary structure changes in a second Per-Arnt-Sim domain mediate intramolecular redox signal relay in the NifL regulatory protein. Mol Microbiol 75:61–75PubMedCrossRefGoogle Scholar
  40. Stivala A, Wybrow M, Wirth A, Whisstock J, Stuckey P (2011) Automatic generation of protein structure cartoons with Pro-origami. Bioinformatics 27:3315–3316. doi:10.1093/bioinformatics/btr575 PubMedCrossRefGoogle Scholar
  41. Stolz A, Riefler M, Lomin SN, Achazi K, Romanov GA, Schmülling T (2011) The specificity of cytokinin signalling in Arabidopsis thaliana is mediated by differing ligand affinities and expression profiles of the receptors. Plant J 67:157–168PubMedCrossRefGoogle Scholar
  42. Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506PubMedGoogle Scholar
  43. To JP, Kieber JJ (2008) Cytokinin signaling: two-component and more. Trends Plant Sci 13:85–92PubMedCrossRefGoogle Scholar
  44. Vreede J, van der Horst MA, Hellingwerf KJ, Wim Crielaard W, van Aalten DMF (2003) PAS domains. Common structure and common flexibility. J Biol Chem 278:18434–18439Google Scholar
  45. Wang N, Söderbom F, Anjard C, Shaulsky G, Loomis WF (1999) SDF-2 induction of terminal differentiation in Dictyostelium discoideum is mediated by the membrane-spanning sensor kinase DhkA. Mol Cell Biol 19:4750–4756PubMedGoogle Scholar
  46. Wulfetange K, Lomin SN, Romanov GA, Stolz A, Heyl A, Schmülling T (2011) The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol 156:1808–1818PubMedCrossRefGoogle Scholar
  47. Zhang Z, Hendrickson WA (2010) Structural characterization of the predominant family of histidine kinase sensor domains. J Mol Biol 400:335–353PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Mikhail Yu. Steklov
    • 1
  • Sergey N. Lomin
    • 1
  • Dmitry I. Osolodkin
    • 2
  • Georgy A. Romanov
    • 1
    • 3
  1. 1.K.A. Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  2. 2.Department of ChemistryLomonosov Moscow State UniversityMoscowRussia
  3. 3.A.N. Belozersky Institute of Physico-Chemical Biology MSUMoscowRussia

Personalised recommendations