Almost 25 years ago, an enzyme named zeatin cis-trans isomerase from common bean has been described by Bassil et al. (1993). The partially purified enzyme required an external addition of FAD and dithiothreitol for the conversion of cis-zeatin to its trans- isomer that occurred only under light. Although an existence of this important enzyme involved in the metabolism of plant hormones cytokinins was generally accepted by plant biologists, the corresponding protein and encoding gene have not been identified to date. Based on the original paper, we purified and identified an enzyme from maize, which shows the described zeatin cis-trans isomerase activity. The enzyme belongs to nucleotide pyrophosphatase/phosphodiesterase family, which is well characterized in mammals, but less known in plants. Further experiments with the recombinant maize enzyme obtained from yeast expression system showed that rather than the catalytic activity of the enzyme itself, a non-enzymatic flavin induced photoisomerization is responsible for the observed zeatin cis-trans interconversion in vitro. An overexpression of the maize nucleotide pyrophosphatase/phosphodiesterase gene led to decreased FAD and increased FMN and riboflavin contents in transgenic Arabidopsis plants. However, neither contents nor the ratio of zeatin isomers was altered suggesting that the enzyme is unlikely to catalyze the interconversion of zeatin isomers in vivo. Using enhanced expression of a homologous gene, functional nucleotide pyrophosphatase/phosphodiesterase was also identified in rice.

Department of Molecular Biology Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University OlomoucOlomouc Czechia

Department of Protein Biochemistry and Proteomics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University OlomoucOlomouc Czechia

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Azami-Sardooei Z., França S. C., De Vleesschauwer D., Höfte M. (2010). Riboflavin induces resistance against DOI

Bassil N. V., Mok D. W. S., Mok M. C. (1993). Partial purification of a PubMed DOI PMC

Belli S. I., van Driel I. R., Goding J. W. (1993). Identification and characterization of a soluble form of the plasma cell membrane glycoprotein PC-1 (5′-nucleotide phosphodiesterase). PubMed DOI

Bjellqvist B., Hughes G. J., Pasquali C., Paquet N., Ravier F., Sanchez J. C., et al. (1993). The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. PubMed DOI

Chatnaparat T., Li Z., Korban S. S., Zhao Y. (2015). The bacterial alarmone (p)ppGpp is required for virulence and controls cell size and survival of PubMed DOI PMC

Clough S. J., Bent A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of PubMed DOI

Collier R., Fuchs B., Walter N., Kevin Lutke W., Taylor C. G. (2005). Ex vitro composite plants: an inexpensive, rapid method for root biology. PubMed DOI

Emanuelsson O., Brunak S., von Heijne G., Nielsen H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. PubMed DOI

Ernst O., Zor T. (1996). Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. PubMed DOI

Farré E. M., Geigenberger P., Willmitzer L., Trethewey R. N. (2000). A possible role for pyrophosphate in the coordination of cytosolic and plastidial carbon metabolism within the potato tuber. PubMed DOI PMC

Gajdošová S., Spíchal L., Kamínek M., Hoyerová K., Novák O., Dobrev P. I., et al. (2011). Distribution, biological activities, metabolism, and the conceivable function of PubMed DOI

Galuszka P., Frébort I., Šebela M., Sauer P., Jacobsen S., Peč P. (2001). Cytokinin oxidase or dehydrogenase? Mechanism of the cytokinin degradation in plants. PubMed DOI

Galuszka P., Popelková H., Werner T., Frébortová J., Pospíšilová H., Mik V., et al. (2007). Biochemical characterization of cytokinin oxidases/dehydrogenases from DOI

Giancaspero T. A., Busco G., Panebianco C., Carmone C., Miccolis A., Liuzzi G. M., et al. (2013). FAD synthesis and degradation in the nucleus create a local flavin cofactor pool. PubMed DOI PMC

Gupta R., Brunak S. (2002). Prediction of glycosylation across the human proteome and the correlation to protein function. PubMed DOI

Hedtke B., Alawady A., Albacete A., Kobayashi K., Melzer M., Roitsch T., et al. (2011). Deficiency in riboflavin biosynthesis affects tetrapyrrole biosynthesis in etiolated Arabidopsis tissue. PubMed DOI

Heelis P. F. (1982). The photophysical and photochemical properties of flavins (isoalloxazines). DOI

Hiltunen H.-M., Illarionov B., Hedtke B., Fischer M., Grimm B. (2012). Arabidopsis RIBA proteins: two out of three isoforms have lost their bifunctional activity in riboflavin biosynthesis. PubMed DOI PMC

Hluska T., Dobrev P. I., Tarkowská D., Frébortová J., Zalabák D., Kopečný D., et al. (2016). Cytokinin metabolism in maize: novel evidence of cytokinin abundance, interconversions and formation of a new PubMed DOI

Hou B., Lim E.-K., Higgins G. S., Bowles D. J. (2004). N-Glucosylation of cytokinins by glycosyltransferases of PubMed DOI

Hruz T., Laule O., Szabo G., Wessendorp F., Bleuler S., Oertle L., et al. (2008). Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. PubMed DOI PMC

Jiskrová E., Novák O., Pospíšilová H., Holubová K., Karády M., Galuszka P., et al. (2016). Extra- and intracellular distribution of cytokinins in the leaves of monocots and dicots. PubMed DOI

Joye I. J., Beliën T., Brijs K., Proost P., Soetaert W., Delcour J. A. (2010). Characterization of the first wheat ( DOI

Kakimoto T. (2001). Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. PubMed DOI

Kaneko K., Inomata T., Masui T., Koshu T., Umezawa Y., Itoh K., et al. (2014). Nucleotide pyrophosphatase/phosphodiesterase 1 exerts a negative effect on starch accumulation and growth in rice seedlings under high temperature and CO2 concentration conditions. PubMed DOI PMC

Kato K., Nishimasu H., Okudaira S., Mihara E., Ishitani R., Takagi J., et al. (2012). Crystal structure of Enpp1 an extracellular glycoprotein involved in bone mineralization and insulin signaling. PubMed DOI PMC

Knobloch E., Mandys F., Hodr R., Hujer R., Mader R. (1991). Study of the mechanism of the photoisomerization and photooxidation of bilirubin using a model for the phototherapy of hyperbilirubinemia. PubMed DOI

Krogh A., Larsson B., von Heijne G., Sonnhammer E. L. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. PubMed DOI

Li D., Zhu H., Liu K., Liu X., Leggewie G., Udvardi M., et al. (2002). Purple acid phosphatases of PubMed DOI

Lindner A.-C., Lang D., Seifert M., Podlešáková K., Novák O., Strnad M., et al. (2014). Isopentenyltransferase-1 (IPT1) knockout in Physcomitrella together with phylogenetic analyses of IPTs provide insights into evolution of plant cytokinin biosynthesis. PubMed DOI PMC

Maruta T., Yoshimoto T., Ito D., Ogawa T., Tamoi M., Yoshimura K., et al. (2012). An Arabidopsis FAD pyrophosphohydrolase, AtNUDX23, is involved in flavin homeostasis. PubMed DOI

Miyawaki K., Tarkowski P., Matsumoto-Kitano M., Kato T., Sato S., Tarkowská D., et al. (2006). Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. PubMed DOI PMC

Nanjo Y., Oka H., Ikarashi N., Kaneko K., Kitajima A., Mitsui T., et al. (2006). Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-Golgi to the chloroplast through the secretory pathway. PubMed DOI PMC

Olczak M., Morawiecka B., Watorek W. (2003). Plant purple acid phosphatases - genes, structures and biological function. PubMed

Ouyang M., Ma J., Zou M., Guo J., Wang L., Lu C., et al. (2010). The photosensitive phs1 mutant is impaired in the riboflavin biogenesis pathway. PubMed DOI

Persson B. C., Björk G. R. (1993). Isolation of the gene ( PubMed DOI PMC

Porra R. J., Thompson W. A., Kriedemann P. E. (1989). Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. DOI

Rodríguez-López M., Baroja-Fernández E., Zandueta-Criado A., Pozueta-Romero J. (2000). Adenosine diphosphate glucose pyrophosphatase: a plastidial phosphodiesterase that prevents starch biosynthesis. PubMed DOI PMC

Sakagami H., Aoki J., Natori Y., Nishikawa K., Kakehi Y., Natori Y., et al. (2005). Biochemical and molecular characterization of a novel choline-specific glycerophosphodiester phosphodiesterase belonging to the nucleotide pyrophosphatase/phosphodiesterase family. PubMed DOI

Šebela M., Brauner F., Radová A., Jacobsen S., Havliš J., Galuszka P., et al. (2000). Characterisation of a homogeneous plant aminoaldehyde dehydrogenase. PubMed DOI

Šebela M., Štosová T., Havliš J., Wielsch N., Thomas H., Zdráhal Z., et al. (2006). Thermostable trypsin conjugates for high-throughput proteomics: synthesis and performance evaluation. PubMed DOI

Shine W. E., Loomis W. D. (1974). Isomerization of geraniol and geranyl phosphate by enzymes from carrot and peppermint. DOI

Šmehilová M., Galuszka P., Bilyeu K. D., Jaworek P., Kowalska M., Šebela M., et al. (2009). Subcellular localization and biochemical comparison of cytosolic and secreted cytokinin dehydrogenase enzymes from maize. PubMed DOI

Spanò D., Pintus F., Pes R., Medda R., Floris G. (2011). Purification and characterisation of a soluble nucleotide pyrophosphatase/phosphodiesterase from prickly pear ( DOI

Stefan C., Jansen S., Bollen M. (2005). NPP-type ectophosphodiesterases: unity in diversity. PubMed DOI

Suttle J. C., Banowetz G. M. (2000). Changes in DOI

Svačinová J., Novák O., Plačková L., Lenobel R., Holík J., Strnad M., et al. (2012). A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. PubMed DOI PMC

Takei K., Yamaya T., Sakakibara H. (2004). Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of PubMed DOI

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. PubMed DOI PMC

Thompson J., Higgins D., Gibson T. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. PubMed DOI PMC

Trdá L., Barešová M., Šašek V., Nováková M., Zahajská L., Dobrev P. I., et al. (2017). Cytokinin metabolism of pathogenic fungus PubMed DOI PMC

Veach Y. K., Martin R. C., Mok D. W. S., Malbeck J., Vaňková R., Mok M. C. (2003). PubMed DOI PMC

Werner T., Schmülling T. (2009). Cytokinin action in plant development. PubMed DOI

Wu J., Liu F., Nilsson Å., Duan R.-D. (2004). Pancreatic trypsin cleaves intestinal alkaline sphingomyelinase from mucosa and enhances the sphingomyelinase activity. PubMed DOI

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 PubMed DOI PMC

Zimmermann H., Zebisch M., Sträter N. (2012). Cellular function and molecular structure of ecto-nucleotidases. PubMed DOI PMC

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