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Advances in upstream players of cytokinin phosphorelay: receptors and histidine phosphotransfer proteins

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Abstract

Cytokinins are a class of plant hormones that have been linked to numerous growth and developmental aspects in plants. The cytokinin signal is perceived by sensor histidine kinase receptors and transmitted via histidine phosphotransfer proteins (HPts) to downstream response regulators. Since their discovery, cytokinin receptors have been a focus of interest for many researchers. Ongoing research on these transmembrane receptors has greatly broadened our knowledge in terms of cytokinin–receptor interaction, receptor specificity, receptor cellular localization, and receptor functions in cytokinin related growth and developmental processes. This review focuses on the recent advances on the cytokinin receptors and HPt proteins in Arabidopsis.

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References

  • Acharya B, Assmann S (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462

    Article  PubMed  CAS  Google Scholar 

  • 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 26:579–582

    Article  PubMed  CAS  Google Scholar 

  • Beier D, Gross R (2006) Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9:143–152

    Article  PubMed  CAS  Google Scholar 

  • Bishopp A, Lehesranta S, Vatén A, Help H, El-Showk S, Scheres B, Helariutta K, Mähönen AP, Sakakibara H, Helariutta Y (2011) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21:927–932

    Google Scholar 

  • Brenner WG, Romanov GA, Kollmer I, Burkle L, Schmulling T (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J 44:314–333

    Article  PubMed  CAS  Google Scholar 

  • Caesar K, Thamm AMK, Witthöft J, Elgass K, Huppenberger P, Grefen C, Horak J, Harte K (2011) Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. J Exp Bot 62:5571–5580

    Article  PubMed  CAS  Google Scholar 

  • Cano-Delgado AI, Metzlaff K, Bevan MW (2000) The eli1 mutation reveals a link between cell expansion and secondary cell wall formation in Arabidopsis thaliana. Development 127:3395–3405

    PubMed  CAS  Google Scholar 

  • Catlett NL, Yoder OC, Turgeon BG (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eucaryot Cell 2:1151–1161

    Article  CAS  Google Scholar 

  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544

    Article  PubMed  CAS  Google Scholar 

  • Coba de la Peña T, Cárcamo CB, Almonacid L, Zaballos A, Lucas MM, Balomenos D, Pueyo JJ (2008) A salt stress-responsive cytokinin receptor homologue isolated from Medicago sativa nodules. Planta 227:769–779

    Article  PubMed  Google Scholar 

  • Cutcliffe JW, Hellmann E, Heyl A, Rashotte AM (2011) CRFs form protein–protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain. J Exp Bot 62:4995–5002

    Article  PubMed  CAS  Google Scholar 

  • Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682

    Article  PubMed  CAS  Google Scholar 

  • Deng Y, Dong H, Mu J, Ren B, Zheng B, Ji Z, Yang WC, Liang Y, Zuo J (2010) Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell 22:1232–1248

    Article  PubMed  CAS  Google Scholar 

  • Dortay H, Mehnert N, Bürkle L, Schmülling T, Heyl A (2006) Analysis of protein interactions within the cytokinin-signaling pathway of Arabidopsis thaliana. FEBS J 273:4631–4644

    Article  PubMed  CAS  Google Scholar 

  • Dortay H, Gruhn N, Pfeifer A, Schwerdtner M, Schmülling T, Heyl A (2008) Toward an interaction map of the two-component signaling pathway of Arabidopsis thaliana. J Proteome Res 7:3649–3660

    Article  PubMed  CAS  Google Scholar 

  • Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8:518–525

    Article  PubMed  CAS  Google Scholar 

  • Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693

    Article  PubMed  CAS  Google Scholar 

  • Haberer G, Kieber JJ (2002) Cytokinins: new insights into a classic phytohormone. Plant Physiol 128:354–362

    Article  PubMed  CAS  Google Scholar 

  • 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 A 5:629–633

    Article  CAS  Google Scholar 

  • Hejátko J, Ryu H, Kim GT, Dobesova R, Choi S, Choi SM, Soucek P, Horak J, Pekarova B, Palme K et al (2009) The histidine kinases cytokinin-independent1 and Arabidopsis histidine kinase 2 and 3 regulate vascular tissue development in Arabidopsis shoots. Plant Cell 21:2008–2021

    Article  PubMed  Google Scholar 

  • Heyl A, Schmulling T (2003) Cytokinin signal perception and transduction. Curr Opin Plant Biol 6:480–488

    Article  PubMed  CAS  Google Scholar 

  • Heyl A, Wulfetange K, Pils B, Nielsen N, Romanov GA, Schmulling T (2007) Evolutionary proteomics identifies amino acids essential for ligand-binding of the cytokinin receptor CHASE domain. BMC Evol Biol 7:62–69

    Article  PubMed  Google Scholar 

  • Higuchi M, Pischke MS, Mahonen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101:8821–8826

    Article  PubMed  CAS  Google Scholar 

  • Hoth S, Ikeda Y, Morgante M, Wang X, Zuo J, Hanafey MK, Gaasterland T, Tingey SV, Chua NH (2003) Monitoring genome-wide changes in gene expression in response to endogenous cytokinin reveals targets in Arabidopsis thaliana. FEBS Lett 554:373–380

    Article  PubMed  CAS  Google Scholar 

  • Hothorn M, Dabi T, Chory J (2011) Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat Chem Biol 7:766–768

    Article  PubMed  CAS  Google Scholar 

  • Hradilová J, Brzobohatý B (2007) Expression pattern of the AHP gene family from Arabidopsis thaliana and organ specific alternative splicing in the AHP5 gene. Biol Plant 51:257–267

    Article  Google Scholar 

  • Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271

    Article  PubMed  CAS  Google Scholar 

  • Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–3087

    Article  PubMed  CAS  Google Scholar 

  • Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383–389

    Article  PubMed  CAS  Google Scholar 

  • Inoue T, Higuchi M, Seki M, Hashimoto Y, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Kurata N (2006) Identification and characterization of cytokinin signaling gene families in rice. Gene 382:57–65

    Article  PubMed  CAS  Google Scholar 

  • Jeon J, Kim NY, Kim S, Kang NY, Novak O, Ku SJ, Cho C, Lee DJ, Lee EJ, Strnad M, Kim J (2010) A subset of cytokinin two component signalling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23371–23386

    Article  PubMed  CAS  Google Scholar 

  • Jung KW, Oh SI, Kim YY, Yoo KS, Cui MH, Shin JS (2008) Arabidopsis histidine-containing phosphotransfer factor 4 (AHP4) negatively regulates secondary wall thickening of the anther endothecium during flowering. Mol Cells 25:294–300

    PubMed  CAS  Google Scholar 

  • Kakimoto T (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal-transduction. Science 274:982–985

    Article  PubMed  CAS  Google Scholar 

  • Kakimoto T (1998) Genes involved in cytokinin signal transduction. J Plant Res 111:261–265

    Article  CAS  Google Scholar 

  • Kieber JJ, Schaller GE (2010) The perception of cytokinin: a story 50 years in the making. Plant Physiol 154:487–492

    Article  PubMed  CAS  Google Scholar 

  • Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci USA 103:814–819

    Article  PubMed  CAS  Google Scholar 

  • Lara MEB, Garcia MCG, Fatima T, Ehne R, Lee TK, Proels R, Tanner W, Roitsch T (2004) Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16:1276–1287

    Article  Google Scholar 

  • Le DN, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2011) Genome-wide expression profiling of soybean two-component system genes in soybean root and shoot tissues under dehydration stress. DNA Res 18:17–29

    Article  PubMed  CAS  Google Scholar 

  • Lee RH, Wang CH, Huang LT, Chen SCG (2001) Leaf senescence in rice plants: cloning and characterization of senescence up-regulated genes. J Exp Bot 52:1117–1121

    Article  PubMed  CAS  Google Scholar 

  • Lim PO, Lee IC, Kim J, Kim HJ, Ryu JS, Woo HR, Nam HG (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J Exp Bot 61:1419–1430

    Article  PubMed  CAS  Google Scholar 

  • Lohrmann J, Sweere U, Zabaleta E, Baurle I, Keitel C, Kozma-Bognar L, Brennicke A, Schafer E, Kudla J, Harter K (2001) The response regulator ARR2: a pollenspecific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis. Mol Genet Genomics 265:2–13

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mähönen AP, Bonke M, Kauppinen L, Marjukka R, Benfey PN, Helariutta Y (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14:2938–2943

    Article  PubMed  Google Scholar 

  • Mähönen AP, Higuchi M, Tormakangas K, Miyawaki K, Pischke MS, Sussman MR, Helariutta Y, Kakimoto T (2006) Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr Biol 16:1116–1122

    Article  PubMed  Google Scholar 

  • Merchan F, De Lorenzo L, González-Rizzo S, Niebel A, Manyani H, Frugier F, Sousa C, Crespi M (2007) Identification of regulatory pathways involved in the reacquisition of root growth alter salt stress in Medicago truncatula. Plant J 51:1–17

    Article  PubMed  CAS  Google Scholar 

  • Merewitz E, Gianfagna T, Huang B (2010) Effects of SAG12-ipt and HSP18.2-ipt expression on cytokinin production, root growth and leaf senescence in creeping bentgrass exposed to drought stress. J Am Soc Hortic Sci 135:230–239

    Google Scholar 

  • Mok DW, Mok MC (2001) Cytokinin metabolism and action. Ann Rev Plant Phys Plant Mol Bio 89:89–118

    Article  Google Scholar 

  • Mougel C, Zhulin IB (2001) CHASE: an extracellular sensing domain common to transmembrane receptors from prokaryotes, lower eukaryotes and plants. Trends Biochem Sci 26:582–584

    Article  PubMed  CAS  Google Scholar 

  • Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (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

    Article  PubMed  CAS  Google Scholar 

  • Pareek A, Singh A, Kumar M, Kushwaha HR, Lynn AM, Singla-Pareek SL (2006) Whole-genome analysis of Oryza sativa reveals similar architecture of two component signaling machinery with Arabidopsis. Plant Physiol 142:380–397

    Article  PubMed  CAS  Google Scholar 

  • Pils B, Heyl A (2009) Unraveling the evolution of cytokinin signaling. Plant Physiol 151:782–791

    Article  PubMed  CAS  Google Scholar 

  • Punwani JA, Hutchison CE, Schaller GE, Kieber JJ (2010) The subcellular distribution of the Arabidopsis histidine phosphotransfer proteins is independent of cytokinin signaling. Plant J 62:473–482

    Article  PubMed  CAS  Google Scholar 

  • Quail PH (2002) Photosensory perception and signalling in plant cells: new paradigms? Curr Opin Cell Biol 14:180–188

    Article  PubMed  CAS  Google Scholar 

  • Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282

    Article  PubMed  CAS  Google Scholar 

  • Rashotte AM, Goertzen LR (2010) The CRF domain defines cytokinin response factor proteins in plants. BMC Plant Biol 10:74–83

    Article  PubMed  Google Scholar 

  • Rashotte AM, Carson SD, To JP, Kieber JJ (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol 132:1998–2011

    Article  PubMed  CAS  Google Scholar 

  • Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc Natl Acad Sci USA 103:11081–11085

    Article  PubMed  CAS  Google Scholar 

  • Riefler M, Novak O, Strnad M, Schmulling 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

    Article  PubMed  CAS  Google Scholar 

  • Romanov GA, Spíchal L, Lomin SN, Strnad M, Schmülling T (2005) A live cell hormone-binding assay on transgenic bacteria expressing a eukaryotic receptor protein. Anal Biochem 347:129–134

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Scharein B, Groth G (2011) Phosphorylation alters the interaction of the Arabidopsis phosphotransfer protein AHP1 with its sensor kinase ETR1. PLoS ONE 6:e24173

    Article  PubMed  CAS  Google Scholar 

  • Scharein B, Voet-van-Vormizeele J, Harter K, Groth G (2008) Ethylene signaling: identification of a putative ETR1–AHP1 phosphorelay complex by fluorescence spectroscopy. Anal Biochem 377:72–76

    Article  PubMed  CAS  Google Scholar 

  • Schepens I, Duek P, Fankhauser C (2004) Phytochrome-mediated light signalling in Arabidopsis. Curr Opin Plant Biol 7:564–569

    Article  PubMed  CAS  Google Scholar 

  • Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:419–448

    Article  CAS  Google Scholar 

  • Spíchal L, Rakova NY, Riefler M, Mizuno T, Romanov GA, Strnad M, Schmulling T (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

    Article  PubMed  Google Scholar 

  • Stolz A, Riefler M, Lomin SN, Achazi K, Romanov GA, Schmülling T (2011) The specificity of cytokinin signalling in Arabidopsis thaliana is mediated by differing ligand affinities and expression profiles of the receptors. Plant J 67:157–168

    Article  PubMed  CAS  Google Scholar 

  • Strasser B, Sanchez-Lamas M, Yanovsky MJ, Casal JJ, Cerdan PD (2010) Arabidopsis thaliana life without phytochromes. Proc Natl Acad Sci USA 107:4776–4781

    Article  PubMed  CAS  Google Scholar 

  • Sugawara H, Kawano Y, Hatakeyama T, Yamaya T, Kamiya N, Sakakibara H (2005) Crystal structure of the histidine-containing phosphotransfer protein ZmHP2 from maize. Protein Sci 14:202–208

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Imamura A, Ueguchi C, Mizuno T (1998) Histidine containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol 39:1258–1268

    PubMed  CAS  Google Scholar 

  • Suzuki T, Sakurai K, Imamura A, Nakamura A, Ueguchi C, Mizuno T (2000) Compilation and characterization of histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in plants: AHP signal transducers of Arabidopsis thaliana. Biosci Biotechnol Biochem 6:2486–2489

    Article  Google Scholar 

  • Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, Mizuno T (2001a) The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol 42:107–113

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Sakurai K, Ueguchi C, Mizuno T (2001b) Two types of putative nuclear factors that physically interact with histidine-containing phosphotransfer (Hpt) domains, signaling mediators in His-to-Asp phosphorelay, in Arabidopsis thaliana. Plant Cell Physiol 42:37–45

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Ishikawa K, Yamashino T, Mizuno T (2002) An Arabidopsis histidine-containing phosphotransfer (HPt) factor implicated in phosphorelay signal transduction: overexpression of AHP2 in plants results in hypersensitiveness to cytokinin. Plant Cell Physiol 43:123–129

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Suzuki T, Yamashino T, Mizuno T (2004) Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana. Biosci Biotechnol Biochem 68:462–465

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006) Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis. J Exp Bot 57:2259–2266

    Article  PubMed  CAS  Google Scholar 

  • Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107

    Article  PubMed  CAS  Google Scholar 

  • To JP, Kieber JJ (2008) Cytokinin signaling: two-components and more. Trends Plant Sci 13:85–92

    Article  PubMed  CAS  Google Scholar 

  • Tran LSP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi Shinozaki K (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

    Article  PubMed  CAS  Google Scholar 

  • Ueguchi C, Koizumi H, Suzuki T, Mizuno T (2001a) Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol 42:231–235

    Article  PubMed  CAS  Google Scholar 

  • Ueguchi C, Sato S, Kato T, Tabata S (2001b) The AHK4 gene involved in the cytokinin-signaling pathway as a direct receptor molecule in Arabidopsis thaliana. Plant Cell Physiol 42:751–755

    Article  PubMed  CAS  Google Scholar 

  • Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754

    Article  PubMed  CAS  Google Scholar 

  • Urao T, Miyata S, Yamaguchi-Shinozaki K, Shinozaki K (2000) Possible His to Asp phosphorelay signaling in an Arabidopsis two-component system. FEBS Lett 478:227–232

    Article  PubMed  CAS  Google Scholar 

  • Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538

    Article  PubMed  CAS  Google Scholar 

  • West AH, Stock AM (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26:369–376

    Article  PubMed  CAS  Google Scholar 

  • Wulfetange K, Lomin SN, Romanov GA, Stolz A, Heyl A, Schmülling T (2011) The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol 156:1808–1818

    Article  PubMed  CAS  Google Scholar 

  • Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–1023

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

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We thank all members of the Rashotte laboratory for critical reading of this manuscript.

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Correspondence to Aaron M. Rashotte.

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Communicated by R. Reski.

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Shi, X., Rashotte, A.M. Advances in upstream players of cytokinin phosphorelay: receptors and histidine phosphotransfer proteins. Plant Cell Rep 31, 789–799 (2012). https://doi.org/10.1007/s00299-012-1229-9

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  • DOI: https://doi.org/10.1007/s00299-012-1229-9

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