Cytokinin signaling: two-components and more.

The hormone cytokinin is perceived via a phosphorelay that is similar to the two-component systems with which bacteria sense and respond to environmental stimuli. Characterization of two-component elements in Arabidopsis, maize and rice shows that cytokinin responses are mediated via partially redundant two-component protein families: histidine kinases, histidine phosphotransfer proteins and response regulators, as well as by novel players, such as the cytokinin response factors. Recent studies in the model plant Arabidopsis have revealed that cytokinin regulates these signaling components through a variety of mechanisms, including modulating transcription, controlling phosphorelay and regulating protein localization and stability. Genetic analyses of cytokinin signaling components have clarified the roles of cytokinin signaling in development and revealed novel functions for this 'classic' phytohormone.

[1]  T. Mizuno,et al.  In vivo and in vitro characterization of the ARR11 response regulator implicated in the His-to-Asp phosphorelay signal transduction in Arabidopsis thaliana. , 2003, Plant & cell physiology.

[2]  T. Mizuno,et al.  Comparative Studies of the AHP Histidine-containing Phosphotransmitters Implicated in His-to-Asp Phosphorelay in Arabidopsis thaliana , 2004, Bioscience, biotechnology, and biochemistry.

[3]  S. Tabata,et al.  The AHK4 gene involved in the cytokinin-signaling pathway as a direct receptor molecule in Arabidopsis thaliana. , 2001, Plant & cell physiology.

[4]  T. Baskin,et al.  Stunted plant 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. , 2000, Plant physiology.

[5]  M. Crespi,et al.  The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti[W] , 2006, The Plant Cell Online.

[6]  Takeshi Mizuno,et al.  Combinatorial microarray analysis revealing arabidopsis genes implicated in cytokinin responses through the His->Asp Phosphorelay circuitry. , 2005, Plant & cell physiology.

[7]  T. Mizuno,et al.  Arabidopsis response regulator, ARR22, ectopic expression of which results in phenotypes similar to the wol cytokinin-receptor mutant. , 2004, Plant & cell physiology.

[8]  Ari Pekka Mähönen,et al.  A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. , 2000, Genes & development.

[9]  T. Mizuno,et al.  Comparative studies on the type-B response regulators revealing their distinctive properties in the His-to-Asp phosphorelay signal transduction of Arabidopsis thaliana. , 2004, Plant & cell physiology.

[10]  K. Harter,et al.  The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis , 2004, The EMBO journal.

[11]  T. Mizuno,et al.  Characterization of a Unique GATA Family Gene That Responds to Both Light and Cytokinin in Arabidopsis thaliana , 2007, Bioscience, biotechnology, and biochemistry.

[12]  J. Ecker,et al.  Multiple Type-B Response Regulators Mediate Cytokinin Signal Transduction in Arabidopsisw⃞ , 2005, The Plant Cell Online.

[13]  Renze Heidstra,et al.  Cytokinins Determine Arabidopsis Root-Meristem Size by Controlling Cell Differentiation , 2007, Current Biology.

[14]  H. Sakakibara,et al.  Molecular characterization of His-Asp phosphorelay signaling factors in maize leaves: Implications of the signal divergence by cytokinin-inducible response regulators in the cytosol and the nuclei , 2003, Plant Molecular Biology.

[15]  T. Schmülling,et al.  Biochemical characteristics and ligand-binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/AHK4 as revealed by a direct binding assay. , 2006, Journal of experimental botany.

[16]  F. Skoog,et al.  KINETIN, A CELL DIVISION FACTOR FROM DEOXYRIBONUCLEIC ACID1 , 1955 .

[17]  M. Matsuoka,et al.  Ectopic Expression of KNOTTED1-Like Homeobox Protein Induces Expression of Cytokinin Biosynthesis Genes in Rice1[W] , 2006, Plant Physiology.

[18]  N. Ori,et al.  The role of hormones in shoot apical meristem function. , 2006, Current opinion in plant biology.

[19]  T. Mizuno,et al.  Cellular Localization of the Signaling Components of Arabidopsis His-to-Asp Phosphorelay , 2001, Bioscience, biotechnology, and biochemistry.

[20]  T. Mizuno,et al.  Type-B ARR transcription factors, ARR10 and ARR12, are implicated in cytokinin-mediated regulation of protoxylem differentiation in roots of Arabidopsis thaliana. , 2007, Plant & cell physiology.

[21]  J. Kieber,et al.  Cytokinin Signal Transduction , 2010 .

[22]  Nori Kurata,et al.  Identification and characterization of cytokinin-signalling gene families in rice. , 2006, Gene.

[23]  Ferenc Nagy,et al.  Multiple phytohormones influence distinct parameters of the plant circadian clock , 2006, Genes to cells : devoted to molecular & cellular mechanisms.

[24]  S. Tabata,et al.  The type-A response regulator, ARR15, acts as a negative regulator in the cytokinin-mediated signal transduction in Arabidopsis thaliana. , 2003, Plant & cell physiology.

[25]  Joseph J. Kieber,et al.  Two Genes with Similarity to Bacterial Response Regulators Are Rapidly and Specifically Induced by Cytokinin in Arabidopsis , 1998, Plant Cell.

[26]  Alexander Heyl,et al.  Cytokinin signal perception and transduction. , 2003, Current opinion in plant biology.

[27]  Bogumil J. Karas,et al.  A Cytokinin Perception Mutant Colonized by Rhizobium in the Absence of Nodule Organogenesis , 2007, Science.

[28]  E. Belles-Boix,et al.  The KNAT2 Homeodomain Protein Interacts with Ethylene and Cytokinin Signaling1 , 2002, Plant Physiology.

[29]  T. Mizuno,et al.  Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Tabata,et al.  ARR1, a Transcription Factor for Genes Immediately Responsive to Cytokinins , 2001, Science.

[31]  P. Gantet,et al.  Histidine‐containing phosphotransfer domain extinction by RNA interference turns off a cytokinin signalling circuitry in Catharanthus roseus suspension cells , 2004, FEBS letters.

[32]  Jin-Young Park,et al.  Genome-wide expression profiling of ARABIDOPSIS RESPONSE REGULATOR 7(ARR7) overexpression in cytokinin response , 2007, Molecular Genetics and Genomics.

[33]  K. Harter,et al.  Interaction of the Response Regulator ARR4 with Phytochrome B in Modulating Red Light Signaling , 2001, Science.

[34]  Shin-Han Shiu,et al.  Two-Component Signaling Elements and Histidyl-Aspartyl Phosphorelays† , 2008, The arabidopsis book.

[35]  T. Aoyama,et al.  Cytokinin signal transduction in plant cells , 2003, Journal of Plant Research.

[36]  G. Sandberg,et al.  Arabidopsis KNOXI Proteins Activate Cytokinin Biosynthesis , 2005, Current Biology.

[37]  J. Kieber,et al.  Cytokinin signaling. , 2005, Current opinion in plant biology.

[38]  M. Kojima,et al.  Molecular Characterization of Cytokinin-Responsive Histidine Kinases in Maize. Differential Ligand Preferences and Response to cis-Zeatin1 , 2004, Plant Physiology.

[39]  M. Ouzzani,et al.  Nomenclature for Two-Component Signaling Elements of Rice , 2006, Plant Physiology.

[40]  S. Hake,et al.  Control of phyllotaxy in maize by the abphyl1 gene. , 1999, Development.

[41]  T. Schmülling,et al.  Arabidopsis Cytokinin Receptor Mutants Reveal Functions in Shoot Growth, Leaf Senescence, Seed Size, Germination, Root Development, and Cytokinin Metabolism[W] , 2005, The Plant Cell Online.

[42]  G. Sandberg,et al.  Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis , 2006, Proceedings of the National Academy of Sciences.

[43]  J. Sheen,et al.  Two-component circuitry in Arabidopsis cytokinin signal transduction , 2001, Nature.

[44]  C. R. McClung,et al.  Arabidopsis Response Regulators ARR3 and ARR4 Play Cytokinin-Independent Roles in the Control of Circadian Period[W] , 2005, The Plant Cell Online.

[45]  Masayuki Higuchi,et al.  Cytokinin Signaling and Its Inhibitor AHP6 Regulate Cell Fate During Vascular Development , 2006, Science.

[46]  P. Hedden,et al.  KNOX Action in Arabidopsis Is Mediated by Coordinate Regulation of Cytokinin and Gibberellin Activities , 2005, Current Biology.

[47]  T. Schmülling,et al.  Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem. , 1999, The Plant journal : for cell and molecular biology.

[48]  Alexander Heyl,et al.  Analysis of protein interactions within the cytokinin‐signaling pathway of Arabidopsis thaliana , 2006, The FEBS journal.

[49]  Wolfgang Busch,et al.  WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators , 2005, Nature.

[50]  T. Mizuno,et al.  The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. , 2001, Plant & cell physiology.

[51]  T. Mizuno,et al.  The Arabidopsis sensor His-kinase, AHk4, can respond to cytokinins. , 2001, Plant & cell physiology.

[52]  C. R. McClung,et al.  The out of phase 1 Mutant Defines a Role for PHYB in Circadian Phase Control in Arabidopsis1 , 2002, Plant Physiology.

[53]  J. Ecker,et al.  The Arabidopsis Histidine Phosphotransfer Proteins Are Redundant Positive Regulators of Cytokinin Signaling[W] , 2006, The Plant Cell Online.

[54]  J. Kieber,et al.  Expression Profiling of Cytokinin Action in Arabidopsis1[w] , 2003, Plant Physiology.

[55]  Michael R. Sussman,et al.  Cytokinins Regulate a Bidirectional Phosphorelay Network in Arabidopsis , 2006, Current Biology.

[56]  T. Schmülling,et al.  New insights into the biology of cytokinin degradation. , 2006, Plant biology.

[57]  J. Patrick,et al.  PERCEPTION AND SIGNAL TRANSDUCTION OF CYTOKININS , 2006 .

[58]  T. Mizuno,et al.  An Arabidopsis histidine-containing phosphotransfer (HPt) factor implicated in phosphorelay signal transduction: overexpression of AHP2 in plants results in hypersensitiveness to cytokinin. , 2002, Plant & cell physiology.

[59]  Ann M Stock,et al.  Two-component signal transduction. , 2000, Annual review of biochemistry.

[60]  V. Rubio,et al.  Interallelic complementation at the Arabidopsis CRE1 locus uncovers independent pathways for the proliferation of vascular initials and canonical cytokinin signalling. , 2004, The Plant journal : for cell and molecular biology.

[61]  Jitendra P Khurana,et al.  Bmc Plant Biology Molecular Characterization and Differential Expression of Cytokinin-responsive Type-a Response Regulators in Rice (oryza Sativa) , 2005 .

[62]  S. Tabata,et al.  A Gain-of-Function Mutation in a Cytokinin Receptor Triggers Spontaneous Root Nodule Organogenesis , 2007, Science.

[63]  Kazuo Shinozaki,et al.  Identification of CRE1 as a cytokinin receptor from Arabidopsis , 2001, Nature.

[64]  Hitoshi Sakakibara,et al.  Cytokinins: activity, biosynthesis, and translocation. , 2006, Annual review of plant biology.

[65]  M. Kojima,et al.  Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. , 2007, Plant & cell physiology.

[66]  M. Kumar,et al.  Whole-Genome Analysis of Oryza sativa Reveals Similar Architecture of Two-Component Signaling Machinery with Arabidopsis1[W] , 2006, Plant Physiology.

[67]  J. Kieber,et al.  Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. , 2000, Plant physiology.

[68]  Ann M Stock,et al.  Histidine kinases and response regulator proteins in two-component signaling systems. , 2001, Trends in biochemical sciences.

[69]  J. Kieber,et al.  A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[70]  J. Kieber,et al.  Cytokinin Regulates Type-A Arabidopsis Response Regulator Activity and Protein Stability via Two-Component Phosphorelay[W] , 2007, The Plant Cell Online.

[71]  M. Mok,et al.  CYTOKININ METABOLISM AND ACTION. , 2003, Annual review of plant physiology and plant molecular biology.

[72]  Peter J. Davies,et al.  PLANT HORMONES: Biosynthesis, Signal Transduction, Action , 2010 .

[73]  I. C. Lee,et al.  Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[74]  R. Amasino,et al.  Inhibition of Leaf Senescence by Autoregulated Production of Cytokinin , 1995, Science.

[75]  Ming Chen,et al.  The two-component signal system in rice (Oryza sativa L.): a genome-wide study of cytokinin signal perception and transduction. , 2007, Genomics.

[76]  J. Ecker,et al.  Type-A Arabidopsis Response Regulators Are Partially Redundant Negative Regulators of Cytokinin Signaling Online version contains Web-only data. , 2004, The Plant Cell Online.

[77]  S. Tabata,et al.  Histidine Kinase Homologs That Act as Cytokinin Receptors Possess Overlapping Functions in the Regulation of Shoot and Root Growth in Arabidopsis , 2004, The Plant Cell Online.

[78]  N. McRoberts,et al.  Plants and biotrophs: a pivotal role for cytokinins? , 2006, Trends in plant science.

[79]  Hitoshi Sakakibara,et al.  Interactions between nitrogen and cytokinin in the regulation of metabolism and development. , 2006, Trends in plant science.

[80]  D. Jackson,et al.  Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1 , 2004, Nature.

[81]  D. Mok.  Cytokinins: Chemistry, Activity, and Function , 1994 .

[82]  Ari Pekka Mähönen,et al.  In planta functions of the Arabidopsis cytokinin receptor family. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[83]  Valérie Laucou,et al.  Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014928 , 2003, The Plant Cell Online.

[84]  T. Mizuno,et al.  Circadian-Associated Rice Pseudo Response Regulators (OsPRRs): Insight into the Control of Flowering Time , 2005, Bioscience, biotechnology, and biochemistry.

[85]  J. Kyozuka,et al.  Direct control of shoot meristem activity by a cytokinin-activating enzyme , 2007, Nature.

[86]  Takashi Aoyama,et al.  ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. , 2007, Plant & cell physiology.

[87]  Q. Qian,et al.  Cytokinin Oxidase Regulates Rice Grain Production , 2005, Science.