In plants, the multistep phosphorelay (MSP) pathway mediates a range of regulatory processes, including those activated by cytokinins. The cross talk between cytokinin response and light has been known for a long time. However, the molecular mechanism underlying the interaction between light and cytokinin signaling remains elusive. In the screen for upstream regulators we identified a LONG PALE HYPOCOTYL (LPH) gene whose activity is indispensable for spatiotemporally correct expression of CYTOKININ INDEPENDENT1 (CKI1), encoding the constitutively active sensor His kinase that activates MSP signaling. lph is a new allele of HEME OXYGENASE1 (HY1) that encodes the key protein in the biosynthesis of phytochromobilin, a cofactor of photoconvertible phytochromes. Our analysis confirmed the light-dependent regulation of the CKI1 expression pattern. We show that CKI1 expression is under the control of phytochrome A (phyA), functioning as a dual (both positive and negative) regulator of CKI1 expression, presumably via the phyA-regulated transcription factors (TF) PHYTOCHROME INTERACTING FACTOR3 and CIRCADIAN CLOCK ASSOCIATED1. Changes in CKI1 expression observed in lph/hy1-7 and phy mutants correlate with misregulation of MSP signaling, changed cytokinin sensitivity, and developmental aberrations that were previously shown to be associated with cytokinin and/or CKI1 action. Besides that, we demonstrate a novel role of phyA-dependent CKI1 expression in the hypocotyl elongation and hook development during skotomorphogenesis. Based on these results, we propose that the light-dependent regulation of CKI1 provides a plausible mechanistic link underlying the well-known interaction between light- and cytokinin-controlled plant development.

CEITEC Central European Institute of Technology and National Centre for Biomolecular Research Masaryk University CZ 62500 Brno Czech Republic

Zobrazit více v PubMed

Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293: 880–883 PubMed

Alconada Magliano T, Casal JJ (2004) Pre-germination seed-phytochrome signals control stem extension in dark-grown Arabidopsis seedlings. Photochem Photobiol Sci 3: 612–616 PubMed

Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI (2005) Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56: 1535–1544 PubMed

Aloni R, Langhans M, Aloni E, Ullrich CI (2004) Role of cytokinin in the regulation of root gravitropism. Planta 220: 177–182 PubMed

Al-Sady B, Ni W, Kircher S, Schäfer E, Quail PH (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell 23: 439–446 PubMed

Altamura MM, Possenti M, Matteucci A, Baima S, Ruberti I, Morelli G (2001) Development of the vascular system in the inflorescence stem of Arabidopsis. New Phytol 151: 381–389

Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, Etheridge N, Argyros DA, Mason MG, Kieber JJ, Schaller GE (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20: 2102–2116 PubMed PMC

Barlow PW, Fisahn J, Yazdanbakhsh N, Moraes TA, Khabarova OV, Gallep CM (2013) Arabidopsis thaliana root elongation growth is sensitive to lunisolar tidal acceleration and may also be weakly correlated with geomagnetic variations. Ann Bot (Lond) 111: 859–872 PubMed PMC

Bauer D, Viczián A, Kircher S, Nobis T, Nitschke R, Kunkel T, Panigrahi KC, Adám E, Fejes E, Schäfer E, Nagy F (2004) Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16: 1433–1445 PubMed PMC

Bolle C, Koncz C, Chua NH (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev 14: 1269–1278 PubMed PMC

Boylan MT, Quail PH (1991) Phytochrome A overexpression inhibits hypocotyl elongation in transgenic Arabidopsis. Proc Natl Acad Sci USA 88: 10806–10810 PubMed PMC

Brandstatter I, Kieber JJ (1998) Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell 10: 1009–1019 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, Romanov GA, Köllmer I, Bürkle L, Schmülling 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 PubMed

Cerdán PD, Chory J (2003) Regulation of flowering time by light quality. Nature 423: 881–885 PubMed

Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38: 87–117 PubMed

Chen S, Lory N, Stauber J, Hoecker U (2015) Photoreceptor specificity in the light-induced and COP1-mediated rapid degradation of the repressor of photomorphogenesis SPA2 in Arabidopsis. PLoS Genet 11: e1005516. PubMed PMC

Chory J, Peto CA, Ashbaugh M, Saganich R, Pratt L, Ausubel F (1989) Different roles for phytochrome in etiolated and green plants deduced from characterization of Arabidopsis thaliana mutants. Plant Cell 1: 867–880 PubMed PMC

Chory J, Reinecke D, Sim S, Washburn T, Brenner M (1994) A role for cytokinins in de-etiolation in Arabidopsis (det mutants have an altered response to cytokinins). Plant Physiol 104: 339–347 PubMed PMC

Correll MJ, Kiss JZ (2005) The roles of phytochromes in elongation and gravitropism of roots. Plant Cell Physiol 46: 317–323 PubMed

Cotton JL, Ross CW, Byrne DH, Colbert JT (1990) Down-regulation of phytochrome mRNA abundance by red light and benzyladenine in etiolated cucumber cotyledons. Plant Mol Biol 14: 707–714 PubMed

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 PubMed PMC

Davis SJ, Bhoo SH, Durski AM, Walker JM, Vierstra RD (2001) The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol 126: 656–669 PubMed PMC

Davis SJ, Kurepa J, Vierstra RD (1999) The Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases. Proc Natl Acad Sci USA 96: 6541–6546 PubMed PMC

De Simone S, Oka Y, Inoue Y (2000) Effect of light on root hair formation in Arabidopsis thaliana phytochrome-deficient mutants. J Plant Res 1131: 63–69

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 PubMed

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 PubMed PMC

Dobisová T, Hejátko J (2014) Automated microscopy in forward genetic screening of Arabidopsis. Methods Mol Biol 1080: 53–66 PubMed

Emborg TJ, Walker JM, Noh B, Vierstra RD (2006) Multiple heme oxygenase family members contribute to the biosynthesis of the phytochrome chromophore in Arabidopsis. Plant Physiol 140: 856–868 PubMed PMC

Flis A, Fernández AP, Zielinski T, Mengin V, Sulpice R, Stratford K, Hume A, Pokhilko A, Southern MM, Seaton DD, McWatters HG, Stitt M, et al. (2015) Defining the robust behaviour of the plant clock gene circuit with absolute RNA timeseries and open infrastructure. Open Biol 5: 5 PubMed PMC

Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61: 11–24 PubMed PMC

Green RM, Tobin EM (1999) Loss of the circadian clock-associated protein 1 in Arabidopsis results in altered clock-regulated gene expression. Proc Natl Acad Sci USA 96: 4176–4179 PubMed PMC

Gutiérrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci USA 105: 4939–4944 PubMed PMC

Hall A, Kozma-Bognár L, Tóth R, Nagy F, Millar AJ (2001) Conditional circadian regulation of PHYTOCHROME A gene expression. Plant Physiol 127: 1808–1818 PubMed PMC

Hejátko J, Pernisová M, Eneva T, Palme K, Brzobohatý B (2003) The putative sensor histidine kinase CKI1 is involved in female gametophyte development in Arabidopsis. Mol Genet Genomics 269: 443–453 PubMed

Hejátko J, Ryu H, Kim GT, Dobesová R, Choi S, Choi SM, Soucek P, Horák J, Pekárová B, Palme K, Brzobohaty B, Hwang I (2009) The histidine kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots. Plant Cell 21: 2008–2021 PubMed PMC

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

Hisada A, Hanzawa H, Weller JL, Nagatani A, Reid JB, Furuya M (2000) Light-induced nuclear translocation of endogenous pea phytochrome A visualized by immunocytochemical procedures. Plant Cell 12: 1063–1078 PubMed PMC

Hoecker U, Xu Y, Quail PH (1998) SPA1: a new genetic locus involved in phytochrome A-specific signal transduction. Plant Cell 10: 19–33 PubMed PMC

Hudson ME, Quail PH (2003) Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol 133: 1605–1616 PubMed PMC

Hughes J. (2013) Phytochrome cytoplasmic signaling. Annu Rev Plant Biol 64: 377–402 PubMed

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 PubMed PMC

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

Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63: 353–380 PubMed

Immanen J, Nieminen K, Smolander OP, Kojima M, Alonso Serra J, Koskinen P, Zhang J, Elo A, Mähönen AP, Street N, Bhalerao RP, Paulin L, et al. (2016) Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr Biol 26: 1990–1997 PubMed

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

Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91: 29–66 PubMed

Kieber JJ, Schaller GE (2014) Cytokinins. Arabidopsis Book 12: e0168. PubMed PMC

Kim L, Kircher S, Toth R, Adam E, Schäfer E, Nagy F (2000) Light-induced nuclear import of phytochrome-A:GFP fusion proteins is differentially regulated in transgenic tobacco and Arabidopsis. Plant J 22: 125–133 PubMed

Kircher S, Gil P, Kozma-Bognár L, Fejes E, Speth V, Husselstein-Muller T, Bauer D, Adám E, Schäfer E, Nagy F (2002) Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14: 1541–1555 PubMed PMC

Koornneef M, Rolff E, Spruit CJP (1980) Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L) Heynh. Z Pflanzenphysiol 100: 147–160

Kraepiel Y, Jullien M, Cordonnier-Pratt MM, Pratt L (1994) Identification of two loci involved in phytochrome expression in Nicotiana plumbaginifolia and lethality of the corresponding double mutant. Mol Gen Genet 242: 559–565 PubMed

Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14: 2366–2376 PubMed PMC

Leivar P, Monte E (2014) PIFs: systems integrators in plant development. Plant Cell 26: 56–78 PubMed PMC

Li J, Li G, Wang H, Wang Deng X (2011) Phytochrome signaling mechanisms. Arabidopsis Book 9: e0148. 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 Arabidopsis. Curr Biol 16: 1116–1122 PubMed

Martínez-García JF, Huq E, Quail PH (2000) Direct targeting of light signals to a promoter element-bound transcription factor. Science 288: 859–863 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

Mizuno K, Shimokor M, Komamine A (1971) Vessel element formation in cultured carrot-root phloem slices. Plant Cell Physiol 12: 823

Müller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453: 1094–1097 PubMed PMC

Muramoto T, Kohchi T, Yokota A, Hwang I, Goodman HM (1999) The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11: 335–348 PubMed PMC

Nagatani A, Reed JW, Chory J (1993) Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A. Plant Physiol 102: 269–277 PubMed PMC

Nagel DH, Doherty CJ, Pruneda-Paz JL, Schmitz RJ, Ecker JR, Kay SA (2015) Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis. Proc Natl Acad Sci USA 112: E4802–E4810 PubMed PMC

Nagel DH, Kay SA (2012) Complexity in the wiring and regulation of plant circadian networks. Curr Biol 22: R648–R657 PubMed PMC

Ni W, Xu SL, Chalkley RJ, Pham TN, Guan S, Maltby DA, Burlingame AL, Wang ZY, Quail PH (2013) Multisite light-induced phosphorylation of the transcription factor PIF3 is necessary for both its rapid degradation and concomitant negative feedback modulation of photoreceptor phyB levels in Arabidopsis. Plant Cell 25: 2679–2698 PubMed PMC

Nicol JW, Helt GA, Blanchard SG Jr., Raja A, Loraine AE (2009) The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25: 2730–2731 PubMed PMC

Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K, Tähtiharju S, Elo A, Decourteix M, Ljung K, Bhalerao R, Keinonen 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 Arabidopsis. Plant Cell 16: 1365–1377 PubMed PMC

Obayashi T, Okamura Y, Ito S, Tadaka S, Aoki Y, Shirota M, Kinoshita K (2014) ATTED-II in 2014: evaluation of gene coexpression in agriculturally important plants. Plant Cell Physiol 55: e6. PubMed PMC

Parks BM, Quail PH (1991) Phytochrome-deficient hy1 and hy2 long hypocotyl mutants of Arabidopsis are defective in phytochrome chromophore biosynthesis. Plant Cell 3: 1177–1186 PubMed PMC

Pernisová M, Klíma P, Horák J, Válková M, Malbeck J, Soucek P, Reichman P, Hoyerová K, Dubová J, Friml J, Zazímalová E, Hejátko J (2009) Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proc Natl Acad Sci USA 106: 3609–3614 PubMed PMC

Pfeiffer A, Janocha D, Dong Y, Medzihradszky A, Schöne S, Daum G, Suzaki T, Forner J, Langenecker T, Rempel E, Schmid M, Wirtz M, et al. (2016) Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. eLife 5: 5 PubMed PMC

Pischke MS, Jones LG, Otsuga D, Fernandez DE, Drews GN, Sussman MR (2002) An Arabidopsis histidine kinase is essential for megagametogenesis. Proc Natl Acad Sci USA 99: 15800–15805 PubMed PMC

Pruneda-Paz JL, Kay SA (2010) An expanding universe of circadian networks in higher plants. Trends Plant Sci 15: 259–265 PubMed PMC

Qamaruddin M, Tillberg E (1989) Rapid effects of red light on the isopentenyladenosine content in scots pine seeds. Plant Physiol 91: 5–8 PubMed PMC

Quail PH, Boylan MT, Parks BM, Short TW, Xu Y, Wagner D (1995) Phytochromes: photosensory perception and signal transduction. Science 268: 675–680 PubMed

Raz V, Ecker JR (1999) Regulation of differential growth in the apical hook of Arabidopsis. Development 126: 3661–3668 PubMed

Reed JW, Nagatani A, Elich TD, Fagan M, Chory J (1994) Phytochrome A and Phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol 104: 1139–1149 PubMed PMC

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 PubMed PMC

Rockwell NC, Su YS, Lagarias JC (2006) Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol 57: 837–858 PubMed PMC

Rösler J, Jaedicke K, Zeidler M (2010) Cytoplasmic phytochrome action. Plant Cell Physiol 51: 1248–1254 PubMed

Sakai H, Honma T, Aoyama T, Sato S, Kato T, Tabata S, Oka A (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294: 1519–1521 PubMed

Sentandreu M, Martín G, González-Schain N, Leivar P, Soy J, Tepperman JM, Quail PH, Monte E (2011) Functional profiling identifies genes involved in organ-specific branches of the PIF3 regulatory network in Arabidopsis. Plant Cell 23: 3974–3991 PubMed PMC

Sharrock RA, Clack T (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol 130: 442–456 PubMed PMC

Smet D, Žádníková P, Vandenbussche F, Benková E, van der Straeten D (2014) Dynamic infrared imaging analysis of apical hook development in Arabidopsis: the case of brassinosteroids. New Phytol 202: 1398–1411 PubMed

Stephenson PG, Fankhauser C, Terry MJ (2009) PIF3 is a repressor of chloroplast development. Proc Natl Acad Sci USA 106: 7654–7659 PubMed PMC

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

Sweere U, Eichenberg K, Lohrmann J, Mira-Rodado V, Bäurle I, Kudla J, Nagy F, Schafer E, Harter K (2001) Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294: 1108–1111 PubMed

Tepperman JM, Hwang YS, Quail PH (2006) phyA dominates in transduction of red-light signals to rapidly responding genes at the initiation of Arabidopsis seedling de-etiolation. Plant J 48: 728–742 PubMed

Terry MJ, Kendrick RE (1999) Feedback inhibition of chlorophyll synthesis in the phytochrome chromophore-deficient aurea and yellow-green-2 mutants of tomato. Plant Physiol 119: 143–152 PubMed PMC

Tóth R, Kevei E, Hall A, Millar AJ, Nagy F, Kozma-Bognár L (2001) Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiol 127: 1607–1616 PubMed PMC

Tsugeki R, Fedoroff NV (1999) Genetic ablation of root cap cells in Arabidopsis. Proc Natl Acad Sci USA 96: 12941–12946 PubMed PMC

Vinti G, Hills A, Campbell S, Bowyer JR, Mochizuki N, Chory J, López-Juez E (2000) Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signalling. Plant J 24: 883–894 PubMed

Vriezen WH, Achard P, Harberd NP, van der Straeten D (2004) Ethylene-mediated enhancement of apical hook formation in etiolated Arabidopsis thaliana seedlings is gibberellin dependent. Plant J 37: 505–516 PubMed

Wang ZY, Kenigsbuch D, Sun L, Harel E, Ong MS, Tobin EM (1997) A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9: 491–507 PubMed PMC

Weller JL, Terry MJ, Rameau C, Reid JB, Kendrick RE (1996) The phytochrome-deficient pcd1 mutant of pea is unable to convert heme to biliverdin IXα. Plant Cell 8: 55–67 PubMed PMC

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

Whitelam GC, Johnson E, Peng J, Carol P, Anderson ML, Cowl JS, Harberd NP (1993) Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5: 757–768 PubMed PMC

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 PubMed

Yoshida S, Mandel T, Kuhlemeier C (2011) Stem cell activation by light guides plant organogenesis. Genes Dev 25: 1439–1450 PubMed PMC

Yuan L, Liu Z, Song X, Johnson C, Yu X, Sundaresan V (2016) The CKI1 histidine kinase specifies the female gametic precursor of the endosperm. Dev Cell 37: 34–46 PubMed

Zádníková P, Petrásek J, Marhavy P, Raz V, Vandenbussche F, Ding Z, Schwarzerová K, Morita MT, Tasaka M, Hejátko J, van der Straeten D, Friml J, et al. (2010) Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137: 607–617 PubMed

Zdarska M, Dobisová T, Gelová Z, Pernisová M, Dabravolski S, Hejátko J (2015) Illuminating light, cytokinin, and ethylene signalling crosstalk in plant development. J Exp Bot 66: 4913–4931 PubMed

Zhang Y, Mayba O, Pfeiffer A, Shi H, Tepperman JM, Speed TP, Quail PH (2013) A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genet 9: e1003244. PubMed PMC

Zubo YO, Yamburenko MV, Selivankina SY, Shakirova FM, Avalbaev AM, Kudryakova NV, Zubkova NK, Liere K, Kulaeva ON, Kusnetsov VV, Börner T (2008) Cytokinin stimulates chloroplast transcription in detached barley leaves. Plant Physiol 148: 1082–1093 PubMed PMC

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

iReenCAM: automated imaging system for kinetic analysis of photosynthetic pigment biosynthesis at high spatiotemporal resolution during early deetiolation

Phytochromes and Their Role in Diurnal Variations of ROS Metabolism and Plant Proteome

Signal Integration in Plant Abiotic Stress Responses via Multistep Phosphorelay Signaling

Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways