Gain-of-Function Mutants of the Cytokinin Receptors AHK2 and AHK3 Regulate Plant Organ Size, Flowering Time and Plant Longevity

. 2017 Mar ; 173 (3) : 1783-1797. [epub] 20170117

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28096190

The phytohormone cytokinin is a regulator of numerous processes in plants. In Arabidopsis (Arabidopsis thaliana), the cytokinin signal is perceived by three membrane-located receptors named ARABIDOPSIS HISTIDINE KINASE2 (AHK2), AHK3, and AHK4/CRE1. How the signal is transmitted across the membrane is an entirely unknown process. The three receptors have been shown to operate mostly in a redundant fashion, and very few specific roles have been attributed to single receptors. Using a forward genetic approach, we isolated constitutively active gain-of-function variants of the AHK2 and AHK3 genes, named repressor of cytokinin deficiency2 (rock2) and rock3, respectively. It is hypothesized that the structural changes caused by these mutations in the sensory and adjacent transmembrane domains emulate the structural changes caused by cytokinin binding, resulting in domain motion propagating the signal across the membrane. Detailed analysis of lines carrying rock2 and rock3 alleles revealed how plants respond to locally enhanced cytokinin signaling. Early flowering time, a prolonged reproductive growth phase, and, thereby, increased seed yield suggest that cytokinin regulates various aspects of reproductive growth. In particular, it counteracts the global proliferative arrest, a correlative inhibition of maternal growth by seeds, an as yet unknown activity of the hormone.

Zobrazit více v PubMed

Ainley WM, McNeil KJ, Hill JW, Lingle WL, Simpson RB, Brenner ML, Nagao RT, Key JL (1993) Regulatable endogenous production of cytokinins up to ‘toxic’ levels in transgenic plants and plant tissues. Plant Mol Biol 22: 13–23 PubMed

Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309: 741–745 PubMed

Bartrina I, Otto E, Strnad M, Werner T, Schmülling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in PubMed PMC

Besnard-Wibaut C. (1981) Effectiveness of gibberellins and 6-benzyladenine on flowering of

Bhargava A, Clabaugh I, To JP, Maxwell BB, Chiang YH, Schaller GE, Loraine A, Kieber JJ (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol 162: 272–294 PubMed PMC

Bhate MP, Molnar KS, Goulian M, DeGrado WF (2015) Signal transduction in histidine kinases: insights from new structures. Structure 23: 981–994 PubMed PMC

Brenner WG, Ramireddy E, Heyl A, Schmülling T (2012) Gene regulation by cytokinin in Arabidopsis. Front Plant Sci 3: 8. PubMed PMC

Brenner WG, Schmülling T (2015) Summarizing and exploring data of a decade of cytokinin-related transcriptomics. Front Plant Sci 6: 29. PubMed PMC

Caesar K, Thamm AMK, Witthöft J, Elgass K, Huppenberger P, Grefen C, Horak J, Harter K (2011) Evidence for the localization of the PubMed PMC

Chervitz SA, Falke JJ (1996) Molecular mechanism of transmembrane signaling by the aspartate receptor: a model. Proc Natl Acad Sci USA 93: 2545–2550 PubMed PMC

Cheung J, Hendrickson WA (2009) Structural analysis of ligand stimulation of the histidine kinase NarX. Structure 17: 190–201 PubMed PMC

Clough SJ, Bent AF (1998) Floral dip: a simplified method for PubMed

Corbesier L, Prinsen E, Jacqmard A, Lejeune P, Van Onckelen H, Périlleux C, Bernier G (2003) Cytokinin levels in leaves, leaf exudate and shoot apical meristem of PubMed

Cortleven A, Nitschke S, Klaumünzer M, Abdelgawad H, Asard H, Grimm B, Riefler M, Schmülling T (2014) A novel protective function for cytokinin in the light stress response is mediated by the ARABIDOPSIS HISTIDINE KINASE2 and ARABIDOPSIS HISTIDINE KINASE3 receptors. Plant Physiol 164: 1470–1483 PubMed PMC

D’Agostino IB, Deruère J, Kieber JJ (2000) Characterization of the response of the PubMed PMC

D’Aloia M, Bonhomme D, Bouché F, Tamseddak K, Ormenese S, Torti S, Coupland G, Périlleux C (2011) Cytokinin promotes flowering of PubMed

Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine PubMed

Dennis ES, Finnegan EJ, Bilodeau P, Chaudhury A, Genger R, Helliwell CA, Sheldon CC, Bagnall DJ, Peacock WJ (1996) Vernalization and the initiation of flowering. Semin Cell Dev Biol 7: 441–448

Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, Jacqmard A, Kilby NJ, Murray JAH (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in PubMed PMC

Dortay H, Mehnert N, Bürkle L, Schmülling T, Heyl A (2006) Analysis of protein interactions within the cytokinin-signaling pathway of PubMed

Efroni I, Han SK, Kim HJ, Wu MF, Steiner E, Birnbaum KD, Hong JC, Eshed Y, Wagner D (2013) Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev Cell 24: 438–445 PubMed PMC

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

Franco-Zorrilla JM, Martín AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138: 847–857 PubMed PMC

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

Gruel J, Landrein B, Tarr P, Schuster C, Refahi Y, Sampathkumar A, Hamant O, Meyerowitz EM, Jönsson H (2016) An epidermis-driven mechanism positions and scales stem cell niches in plants. Sci Adv 2: e1500989. PubMed PMC

Hensel LL, Grbić V, Baumgarten DA, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in PubMed PMC

Hensel LL, Nelson MA, Richmond TA, Bleecker AB (1994) The fate of inflorescence meristems is controlled by developing fruits in Arabidopsis. Plant Physiol 106: 863–876 PubMed PMC

Hewelt A, Prinsen E, Schell J, Van Onckelen H, Schmülling T (1994) Promoter tagging with a promoterless ipt gene leads to cytokinin-induced phenotypic variability in transgenic tobacco plants: implications of gene dosage effects. Plant J 6: 879–891 PubMed

Heyl A, Riefler M, Romanov GA, Schmülling T (2012) Properties, functions and evolution of cytokinin receptors. Eur J Cell Biol 91: 246–256 PubMed

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: 62. PubMed PMC

Higuchi M, Pischke MS, Mähönen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, et al. (2004) In planta functions of the PubMed PMC

Hisanaga T, Kawade K, Tsukaya H (2015) Compensation: a key to clarifying the organ-level regulation of lateral organ size in plants. J Exp Bot 66: 1055–1063 PubMed

Holst K, Schmülling T, Werner T (2011) Enhanced cytokinin degradation in leaf primordia of transgenic PubMed

Hothorn M, Dabi T, Chory J (2011) Structural basis for cytokinin recognition by PubMed PMC

Hwang I, Sheen J (2001) Two-component circuitry in PubMed

Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from PubMed

Jeon J, Kim NY, Kim S, Kang NY, Novák O, Ku SJ, Cho C, Lee DJ, Lee EJ, Strnad M, et al. (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in PubMed PMC

Jung K, Fried L, Behr S, Heermann R (2012) Histidine kinases and response regulators in networks. Curr Opin Microbiol 15: 118–124 PubMed

Kieber JJ, Schaller GE (2014) Cytokinins. The Arabidopsis Book 12: e0168, doi/10.1199/tab.0168 PubMed PMC

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 PubMed PMC

Köllmer I, Novák O, Strnad M, Schmülling T, Werner T (2014) Overexpression of the cytosolic cytokinin oxidase/dehydrogenase (CKX7) from PubMed

Köllmer I, Werner T, Schmülling T (2011) Ectopic expression of different cytokinin-regulated transcription factor genes of PubMed

Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H (2009) Functional analyses of PubMed PMC

Liu YC, Machuca MA, Beckham SA, Gunzburg MJ, Roujeinikova A (2015) Structural basis for amino-acid recognition and transmembrane signalling by tandem Per-Arnt-Sim (tandem PAS) chemoreceptor sensory domains. Acta Crystallogr D Biol Crystallogr 71: 2127–2136 PubMed

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 PubMed

Lomin SN, Krivosheev DM, Steklov MY, Arkhipov DV, Osolodkin DI, Schmülling T, Romanov GA (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 PubMed PMC

Mähönen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the PubMed PMC

Mähönen AP, Higuchi M, Törmäkangas K, Miyawaki K, Pischke MS, Sussman MR, Helariutta Y, Kakimoto T (2006) Cytokinins regulate a bidirectional phosphorelay network in PubMed

Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of PubMed

Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004) A novel regulatory pathway of sulfate uptake in PubMed

Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Václavíková K, Miyawaki K, Kakimoto T (2008) Cytokinins are central regulators of cambial activity. Proc Natl Acad Sci USA 105: 20027–20031 PubMed PMC

Michniewicz M, Kamienska A (1967) Effect of kinetin on the content of endogenous gibberellins in germinating seeds of some plant species. Naturwissenschaften 54: 372 PubMed

Miwa K, Ishikawa K, Terada K, Yamada H, Suzuki T, Yamashino T, Mizuno T (2007) Identification of amino acid substitutions that render the PubMed

Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in PubMed

Moore JO, Hendrickson WA (2009) Structural analysis of sensor domains from the TMAO-responsive histidine kinase receptor TorS. Structure 17: 1195–1204 PubMed

Müller B, Sheen J (2007) Advances in cytokinin signaling. Science 318: 68–69 PubMed

Niemann MCE, Bartrina I, Ashikov A, Weber H, Novák O, Spíchal L, Strnad M, Strasser R, Bakker H, Schmülling T, et al. (2015) PubMed PMC

Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K, Tähtiharju S, Elo A, Decourteix M, Ljung K, et al. (2008) Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA 105: 20032–20037 PubMed PMC

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 PubMed PMC

Noodén LD, Penney JP (2001) Correlative controls of senescence and plant death in PubMed

Novák O, Hauserová E, Amakorová P, Dolezal K, Strnad M (2008) Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69: 2214–2224 PubMed

Richmond AE, Lang A (1957) Effect of kinetin on protein content and survival of detached

Riefler M, Novak O, Strnad M, Schmülling T (2006) PubMed PMC

Romanov GA, Lomin SN, Schmülling T (2006) Biochemical characteristics and ligand-binding properties of PubMed

Rupp HM, Frank M, Werner T, Strnad M, Schmülling T (1999) Increased steady state mRNA levels of the PubMed

Shimizu-Sato S, Tanaka M, Mori H (2009) Auxin-cytokinin interactions in the control of shoot branching. Plant Mol Biol 69: 429–435 PubMed

Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in PubMed PMC

Spíchal L, Rakova NY, Riefler M, Mizuno T, Romanov GA, Strnad M, Schmülling T (2004) Two cytokinin receptors of PubMed

Steklov MY, Lomin SN, Osolodkin DI, Romanov GA (2013) Structural basis for cytokinin receptor signaling: an evolutionary approach. Plant Cell Rep 32: 781–793 PubMed

Stolz A, Riefler M, Lomin SN, Achazi K, Romanov GA, Schmülling T (2011) The specificity of cytokinin signalling in PubMed

Sun J, Niu QW, Tarkowski P, Zheng B, Tarkowska D, Sandberg G, Chua NH, Zuo J (2003) The Arabidopsis PubMed PMC

Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, Mizuno T (2001) The PubMed

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 PubMed PMC

Ueguchi C, Sato S, Kato T, Tabata S (2001) The PubMed

van der Graaff EE, Hooykaas PJJ, Auer CA (2001) Altered development of

Werner T, Holst K, Pörs Y, Guivarc’h A, Mustroph A, Chriqui D, Grimm B, Schmülling T (2008) Cytokinin deficiency causes distinct changes of sink and source parameters in tobacco shoots and roots. J Exp Bot 59: 2659–2672 PubMed PMC

Werner T, Köllmer I, Bartrina I, Holst K, Schmülling T (2006) New insights into the biology of cytokinin degradation. Plant Biol (Stuttg) 8: 371–381 PubMed

Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic PubMed PMC

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

Wuest SE, Philipp MA, Guthörl D, Schmid B, Grossniklaus U (2016) Seed production affects maternal growth and senescence in Arabidopsis. Plant Physiol 171: 392–404 PubMed PMC

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 PubMed PMC

Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The PubMed

Zürcher E, Müller B (2016) Cytokinin synthesis, signaling, and function: advances and new insights. Int Rev Cell Mol Biol 324: 1–38 PubMed

Zürcher E, Tavor-Deslex D, Lituiev D, Enkerli K, Tarr PT, Müller B (2013) A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol 161: 1066–1075 PubMed PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...