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Schriftzug Angewandte Genetik Collage von Motiven der Angewandten Genetik

Dahlem Research School

Member of Dahlem Centre of Plant Sciences (DCPS)

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Research group Heyl

Research interest

The plant hormone cytokinin plays an important role in many physiological and developmental processes as well as the reaction of plants to abiotic and biotic stress. The cytokinin signal perception and transduction is mediated by a multi-step phospho-relay system, a variation of the classical two-component signaling pathway found in bacteria (Heyl and Schmülling, 2003).

In the current model of this signaling pathway, the binding of cytokinin to the ligand binding domain, the CHASE domain, causes the mainly ER-localized cytokinin receptor histidine kinase (HK) to auto-phosphorylate itself at a conserved histidine residue (Heyl et al., 2007; Wulfetange et al., 2011). Subsequently this signal is transferred within the receptor protein to a canonical aspartate residue of a C-terminal response regulator domain. Afterwards, the phosphoryl signal is transferred to a histidine phospho-transfer protein (HPt), which can translocate to the nucleus, where it activates the type-B response regulators (type-B RRs) by phosphorylation of the response regulator domain (Dortay et al., 2006). These Myb- transcription factors activate the transcription of their target genes, one group of which are the type-A RRs (Heyl et al., 2008). These regulate in a negative feedback loop the activity of cytokinin signaling and represent an internode, linking the cytokinin signaling pathway with other cellular signaling pathways (Gruhn and Heyl, 2013).

Cytokinin signalling scheme
Figure 1: Modified model of the cytokinin signal transduction pathway. A 'core' model for the signal transduction of cytokinin (For review see Gruhn and Heyl, 2013). The different domains shown are labeledaccording to the Pfam database ( RR = response regulator receiver domain (PF00072); Myb-related DNA-binding domain (PF00249); HK = histidine kinase, composed of the histidine kinase A domain (PF00512) and the Histidine kinase-ATPase domain (PF02518);HPT = histidine phosphotransfer protein, contains the Hpt domain (PF01627); CHASE = cyclase histidine kinase associated sensory extracellular (PF03924).

In the Heyl group we are interested to understand the molecular mechanism of the cytokinin signaling system. Towards this goal we currently focus on two areas, the regulation of the transcriptional response to cytokinin and the evolution of the cytokinin signal transduction.

Group members

Former group members


Gruhn, N., Halawa, M., Seidl, M. S., Snel, B., Heyl, A. (2014) A new subfamily of cytokinin receptors is revealed by an analysis of the evolution of the two-component signaling system of plants Plant Physiol. 165, 227-237.

Ramireddy, E., Brenner, W. G., Pfeifer, A., Heyl, A., Schmülling, T. (2013) In planta analysis of a cis-regulatory cytokinin response motif in Arabidopsis and identification of a novel enhancer sequence. Plant Cell Physiol. 54, 1079-1092.

Brandt J., Heyl, A. (2013) AgED: Extraction and Evaluation of Elliptic Fourier Descriptors from Image Data in Phenotype Assessment Applications. In: Proc. Internat. Conf. Bioinfo. Models Methods Algorithms pp. 324-327.

Gruhn, N., Heyl, A. (2013) Updates on the model and the evolution of cytokinin signaling. Curr. Opin. Plant Biol. 16, 569-574.

Heyl, A., Brault, M., Frugier, F., Kuderová, A., Lindner, A.C., Motyka, V., Rashotte, A.M., von Schwartzenberg, K., Vankova, R., Schaller, G.E. (2013) Nomenclature for members of the two-component signaling pathway of plants. Plant Physiol. 161, 1063-1065.

Brenner, W.G., Ramireddy, E., Heyl, A., Schmülling, T. (2012) Gene regulation by cytokinin in Arabidopsis. Front. Plant. Sci. 3, 8.

Wulfetange, K., Lomin, S., Romanov, G.A., Stolz, A., Heyl, A., Schmülling,T. (2011) The cytokinin receptors of Arabidopsis thaliana are located mainly to the endoplasmic reticulum. Plant Physiol. 156: 1653-1654.

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

Banks, J.A., Nishiyama, T., Hasebe, M., Bowman, J.L., Gribskov, M., De Pam-Philis, C., Albert, V.A., Aono, N., Aoyama, T., Ambrose, B.A., Ashton, N.W., Axtell, M.J., Barker, E., Barker, M.S., Benntzen, J.L., Bonawitz, N.D., Chap-Ple, C., Cheng, C., Correa, L.G., Dacre, M., Debarry, J., Dreyer, I., Elias, M., Engstrom, E.M., Estelle, M., Feng, L., Finet, C., Floyd, S.K., Frommer, W.B., Fujita, T., Gramzow, L., Gutensohn, M., Harholt, J., Hattori, M., Heyl, A., Hirai, T., Hiwatashi, Y., Ishikawa, M., Iwata, M., Karol, K.G., Köhler, B., Kolukisaoglu, U., Kubo, M., Kurata, T., Lalonde, S., Li, K., Li, Y., Litt, A., Lyons, E., Man-Ning, G., Maruyama, T., Michael, T.P., Mikami, K., Miyazaki, S., MOorinaga, S., Murata, T., Müller-Röber, B., Nelson, D.R., Obara, M., Oguri, Y., Olmstead, R.G., Onodera, N., Petersen, B.L., Pils, B., Prigge, M., Rensing, S.A., Riaño-Pachón, D.M., Roberts, A.W., Sato, Y., Scheller, H.V., Schulz, B., Schulz, C., Shakirov, E.V., Shibagaki, N., Shinohara, N., Shippen, D.E., Sørensen, I., So-Tooka, R., Sugimoto, N., Sugita, M., Sumikawa, N., Tanurdzic, M., Theissen, G., Ulvskov, P., Wakazuki, S., Weng, J.K., Willats, W.W., Wipf, D., Wolf, P.G., Yang, L., Zimmer, A.D., Zhu, Q., Mitros, T., Hellsten, U., Loqué, D., Otillar, R., Salamov, A., Schmutz, J., Shapiro, H., Lindquist, E., Lucas, S., Rokhsar, D., Grigoriev, I.V. (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332: 960-963.

Heyl, A., Riefler, M., Romanov, G.A., Schmülling, T. (2011) Properties, functions and evolution of cytokinin receptors. Eur. J. Cell Biol. 91: 246-256

Wulfetange, K., Saenger, W., Schmülling, T., Heyl, A. (2011) E. coli-based cell-free expression, purification and characterization of the membrane-bound ligand-binding CHASE-TM domain of the cytokinin receptor CRE1/AHK4 of Arabidopsis thaliana. Mol. Biotechnol. 47: 211-219.

Twardziok, S., Siebert, H., Heyl, A. (2010) Stochasticity in reactions: a probabilistic Boolean modeling approach. In: Proc. 8th Internat. Conf. Comput. Method Systems Biology, CMSB'10: 76-85.

Hellmann, E., Gruhn, N., Heyl, A. (2010) The more, the merrier: Cytokinin signaling beyond Arabidopsis. Plant Signal. Behav. 5: 1384-1390.

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

Dortay, H., Gruhn, N., Pfeifer, A., Schwerdtner, M., Schmülling,T T., Heyl, A. (2008) Towards an interaction map of the two-component signaling pathway of Arabidopsis thaliana. J. Proteome Res. , 73, 3649-3660

Heyl, A. , Ramireddy, E., Brenner, W., Riefler, M., Allemeersch, J., Schmülling,T T. (2008) Ectopic expression of the dominant transcriptional silencer gene ARR1-SRDX in Arabidopsis suppresses pleiotropic cytokinin activities. Plant Physiol. 147, 1380-1395

Romanov, G., Lomin, S., Rakova, N., Heyl, A. , Schmülling,T T. (2008) Does NO play a role in Cytokinin signal transduction? FEBS Letters 582, 874-880


Rensing, S.A., Lang, D., Zimmer, A.D., Terry, A., Salamov, A., Shapiro, H., Nischiyama, T., Perroud, P.F., Lindquist, E.A., Kamisugi, Y., Tanahashi, T., Sakakibara, K., Fujita, T., Oishi, K., Shin, I.T., Kuroki, Y., Toyoda, A., Suzuki, Y., Hashimotot, S., Yamaguchi, K., Sugano, S., Kohora, Y., Fujiyama, A., Anterola, A., Aoki, S., Ashton, N., Barbazuk, W.B., Barker, E., Bennetzen, J.L., Blankenship, R., Cho, S.H., Dutscher, S.K., Estelle, M., Fawcett, J.A., Gundlach, H., Hanada, K., Heyl, A. , Hicks, K.A., Hughes, J., Lohr, M., Mayer, K.,Melkozernov, A., Murata, T., Nelson, D.R., Pils, B., Prigge, M., Reiss, B., Renner, T., Rombauts, S., Rushton, P.J., Sanderfoot, A., Schween, G., Shiu, S.H., Stueber, K., Theodoulou, F.L., Tu, H., Van De Peer, Y., Verrier, P.J., Waters, E., Wood, A., Yang, L., Cove, D., Cuming, A.C., Hasebe, M., Lucas, S., Mischler, B.D., Reski, R., Grigoriev, I.V., Quatrano, R.S., Boore, J.L. (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69

Riefler, M., Werner, T., Heyl, A. (2007) Cytokinins. In: Encyclopedia of Life Sciences. John Wiley & Sons, Ltd: Chichester, p369-376

Heyl, A. , Wulfetange, K., Pils, B., Nielsen, N., Romanov, G., Schmülling,T. (2007) Evolutionary proteomics identifies ligand-binding amino acids of the cytokinin receptor CHASE domain. BMC Evolut. Biol. 7, 62-70.

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.

(*awarded with the FEBS Journal Young Investigator Award)

Heyl, A. , Werner, T., Schmülling,T T. (2006) Cytokinin metabolism and signal transduction. In: Plant hormone signaling, Annual Plant Reviews (Hedden, P., Thomas, S., eds) . Blackwell Publishing Ltd., Oxford. pp. 93-123.

Bürkle, L., Meyer, S., Dortay, H., Lehrach, H., Heyl, A. (2005) In vitro recombination cloning of entire cDNA libraries in Arabidopsis thaliana and its application to the yeast two-hybrid system. Funct. Integr. Genomics. 5, 175-183.

Heyl, A. and Schmülling,T T. (2003) Cytokinin signal perception and transduction. Curr. Opin. Plant Biol. 6, 480-488.

Heyl, A. , Muth, J., Santadrea, G., O'Conell, T., Serna, A., Thompson, R.D. (2001) A transcript encoding a nucleic acid-binding protein specifically expressed in maize seeds. Mol. Genet. Genomics, 266:180-189.

Heyl, A. , Muth, J., Ficker, M., Thompson, R.D. (1997) Use of the One-Hybrid system to isolate a novel plant transcription factor. Biol. Chem. , 378, Special Supplement, pp.161.

Quarrie, S.A., Lasic-Jancic, V., Ivanovic, M., Pekic, S., Heyl, A., Landi, P., Lebreton, C., Steed, A. (1997) Molecular Marker Methods to Dissect Drought Resistance in Maize. In: Genetics, Biotechnology and Breeding of Maize and Sorghum. Eds. Tsaftaris, A.S.EUCARPA proceedings. pp. 52-58.

Quarrie, S.A., Heyl, A., Steed, A., Lebreton, C., Lasci-Jancic, V. (1996) QTL analysis of stress responses as a method to study the importance of stress-induced genes. In: A. Leone, S. Grillo (Eds) Genes and their products for tolerance to physical stresses in plants. ESF meeting, Maratea, September 1995, Springer, Berlin pp.141-152.

Quarrie, S.A., Lasic-Jancic V., Ivancic, M., Pekic, S., Lebreton, C., Heyl, A. , Steed, A., Calestani, C. (1996) Molecular Markers as Aids to Breeding more Drought-Resistant Crops. International Symposium Drought and Plant Production , Donji Milanovac, Serbia, pp.43-53.


New publication

An article about the analysis of a cytokinin-responsive gene of Arabidopsis thaliana encoding a novel F-box protein regulating sterol biosynthesis has been published in Journal of Experimental Botany.
May 2017

New publication

A report about constitutively active mutants of the cytokinin receptors AHK2 und AHK3 and their impact on organ size, flowering time, and plant longevity has been published in Plant Physiology.
March 2017

New publication

An article about the role of the transcription factor ERF105 in freezing tolerance and cold acclimation has been published in Plant Cell and Environment.
January 2017

Krolow Award 2016

The Krolow Award 2016 was given to Dr. Anne Cortleven for her work about the role of Cytokinin in the plant response to high light stress.
November 2016
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Updated: 2017-04-23