Moss Biology and Phytohormones - Cytokinins in Physcomitrella

Abstract

Mosses present several advantages for the analysis of phytohormone physiology. Their enormous regeneration capacity, the possibility of controlling their whole life cycle under in vitro culture conditions, as well as the small number of cell types facilitate studies of hormone homeostasis. This review focuses on the metabolism and biosynthesis of cytokinins, mostly summarising data obtained using the moss Physcomitrella patens (Hedw.) B.S.G. which has served as a model system for cytokinin research for many years. A comparison of metabolic differences with respect to seed plants is presented, pointing out an important role of adenosine kinase for the formation of nucleotides during cytokinin interconversion in Physcomitrella. Results on cytokinin biosynthesis in Physcomitrella are summarised with respect to the ove mutants, which can be considered unique in the plant kingdom due to their strong overproduction of cytokinins. The ove phenotype is correlated with both increased activity in early stages of cytokinin biosynthesis as well as increased conversion of cytokinin riboside to the base. Cytokinin interconverting reactions can contribute to the increased levels of cytokinins in ove mutants. Further studies on hormone physiology in moss will help to complete our understanding of hormonal homeostasis by elucidating the situation in an evolutionary early embryophyte.

Key words

Bryophyte - adenosine kinase - biosynthesis - metabolism - cytokinin - Physcomitrella.

References

• 1 Akiyoshi D. E., Klee H., Amasine R. M., Nester E. W., Gordon M. P.. T‐DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis.  Proceedings of the National Academy of Sciences of the USA. (1984);  81 5994-5998
• 2 Allen M., Quin W., Moreau F., Moffatt B.. Adenine phosphoribosyltransferase isoforms of Arabidopsis and their potential contributions to adenine and cytokinin metabolism.  Physiologia Plantarum. (2002);  115 56-68
• 3 Ashton N. W., Cove D. J., Featherstone D. R.. The isolation and physiological analysis of mutants of the moss Physcomitrella patens, which overproduce gametophores.  Planta. (1979);  144 437-442
• 4 Barnes M. F., Tien C. L., Gray J. S.. Biosynthesis of cytokinins by potato cell cultures.  Phytochemistry. (1980);  19 409-412
• 5 Barry G. F., Rogers S. G., Fraley R. T., Brand L.. Identification of a cloned cytokinin biosynthetic gene.  Proceedings of the National Acadamy of Sciences of the USA. (1984);  81 4776-4780
• 6 Bauer L.. Isolierung und Testung einer kinetinartigen Substanz aus Kalluszellen von Laubmoossporophyten.  Zeitschrift für Pflanzenphysiologie. (1966);  54 241-253
• 7 Beutelmann P.. Untersuchungen zur Biosynthese eines Cytokinins in Calluszellen von Laubmoossporophyten.  Planta. (1973);  112 181-189
• 8 Bhatla S. C., Dhingra-Babbar S.. Growth regulating substances in mosses. Chopra, R. N. and Bhatla, S. C. eds. Bryophyte Development: Physiology and Biochemistry. Boca Raton; CRC Press (1990): 79-101
• 9 Bopp M.. The hormonal regulation of protonema development in mosses. II. The first steps of cytokinin action.  Zeitschrift für Pflanzenphysiologie. (1984);  113 435-444
• 10 Bopp M.. Hormones of the moss protonema. Chopra, R. N. and Bhatla, S. C., eds. Bryophyte Development: Physiology and Biochemistry. Boca Raton; CRC Press (1990): 55-77
• 11 Chaudhury A. M., Letham S., Craig S., Dennis E. S.. amp1 - a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive morphogenesis and precocious flowering.  The Plant Journal. (1993);  4 907-916
• 12 Chen C.-M.. Biosynthesis and enzymic regulation of the interconversion of cytokinin. Guern, J. and Peaud-Lenoel, C., eds. Metabolism and Molecular Activities of Cytokinins. Berlin; Springer-Verlag (1981): 34-43
• 13 Chen C.-M.. Cytokinin biosynthesis and interconversion.  Physiologia Plantarum. (1997);  101 665-673
• 14 Chen C., Kristopeit S. M.. Metabolism of cytokinin, deribosylation of cytokinin ribonucleoside by adenosine nucleosidase from wheat germ cells.  Plant Physiology. (1981);  68 1020-1023
• 15 Cove D. J., Ashton N. W.. The hormonal regulation of gametophytic development in bryophytes. Dyer, A. F. and Duckett, J. G., eds. The Experimental Biology of Bryophytes. London; Academic Press (1984): 177-201
• 16 Edwards C. A., Armstrong D. J.. Cytokinin-active ribonucleosides in Phaseolus RNA.  Plant Physiology. (1981);  67 1185-1189
• 17 Featherstone D. R., Cove D. J., Ashton N. W.. Genetic analysis by somatic hybridisation of cytokinin overproducing developmental mutants of the moss, Physcomitrella patens.  Molecular and General Genetics. (1990);  222 217-224
• 18 Ferreira F. J., Kieber J. J.. Cytokinin signaling.  Current Opinion in Plant Biology. (2005);  8 518-525
• 19 Frank W., Decker E. L., Reski R.. Molecular tools to study Physcomitrella patens.  Plant Biology. (2005);  7 220-227
• 20 Futers T. S., Wang T. L., Cove D. J.. Characterisation of a temperature-sensitive gametophore over-producing mutant of the moss, Physcomitrella patens.  Molecular and General Genetics. (1986);  203 529-532
• 21 Golovko A., Sitbon F., Tillberg E., Nicander B.. Identification of a tRNA isopentenyltransferase gene from Arabidopsis thaliana.  Plant Molecular Biology. (2002);  49 161-169
• 22 Gorton B. S., Eakin R. E.. Development of the gametophyte in the moss Tortella caespitosa.  Botanical Gazette. (1957);  119 31-38
• 23 Gray J., Gelvin S. B., Meilan R., Morris R. O.. Transfer RNA is the source of extracellular isopentenyladenine in a Ti-plasmidless strain of Agrobacterium tumefaciens.  Plant Physiology. (1996);  110 431-438
• 24 Haberer G., Kieber J. J.. Cytokinins. New insights into a classic phytohormone.  Plant Physiology. (2002);  128 354-362
• 25 Hahn H., Bopp M.. A cytokinin test with high specifity.  Planta. (1968);  83 115-118
• 26 Hohe A., Reski R.. From axenic spore germination to molecular farming. One century of bryophyte in vitro culture.  Plant Cell Reports. (2005);  23 513-521
• 27 Houba-Hérin N., Pethe C., d'Alayer J., Laloue M.. Cytokinin oxidase from Zea mays, purification, cDNA cloning and expression in moss protoplasts.  The Plant Journal. (1999);  17 615-626
• 28 Jahn H.. Der Einfluss von Kinetin auf die Anlage der Stämmchen von Funaria hygrometrica Sibth.  Flora. (1964);  154 568
• 29 Johri M. M.. Possible origin of hormonal regulation in green plants.  Proceedings of the Indian National Science Academy. (2004);  70 335-365
• 30 Kakimoto T.. Identification of plant cytokinin biosynthetic enzymes as dimethyl diphosphate, ATP/ADP isopentenyltransferases.  Plant and Cell Physiology. (2001);  42 677-685
• 31 Kakimoto T.. Biosynthesis of cytokinins.  Journal of Plant Research. (2003);  116 233-239
• 32 Kaminek M., Motyka V., Vankova R.. Regulation of cytokinin content in plant cells.  Physiologia Plantarum. (1997);  101 689-700
• 33 Koenig R. L., Morris R. O., Polacco J. C.. tRNA is the source of low-level trans-zeatin production in Methylobacterium spp.  Journal of Bacteriology. (2002);  184 1832-1842
• 34 Klämbt D., Holtz J., Helbach M., Maaß H.. Die Biogenese der Cytokinine.  Berichte der Deutschen Botanischen Gesellschaft. (1984);  97 57-65
• 35 Laloue M., Terrine C., Guern J.. Cytokinins: metabolism and biological activity of N⁶-(Δ2-isopentenyl)adenosine and N⁶-(Δ2-isopentenyl)adenine in tobacco cells and callus.  Plant Physiology. (1977);  59 478-483
• 36 Laloue M., Pethe-Terrine C., Guern J.. Uptake and metabolism of cytokinins in tobacco cells: studies in relation to the expression of their biological activities. Guern, J. and Peaud-Leonel, C., eds. Metabolism and Molecular Activities of Cytokinins. Berlin; Springer Verlag (1981): 80-96
• 37 Laloue M., Pethe C.. Dynamics of cytokinin metabolism in tobacco cells. Wareing, P. F., ed. Plant Growth Substances. London; Academic Press (1982): 185-195
• 38 Letham D. S.. Zeatin, a factor inducing cell division from Zea mays.  Life Science. (1963);  8 569-573
• 39 Miller C. O., Skoog F., Okomura F. S., v. Saltza M. H., Strong F. M.. Isolation, structure and synthesis of kinetin, a substance promoting cell division.  Journal of the American Chemical Society. (1956);  78 1345-1350
• 40 Moffatt B., Wang L., Allen M., Stevens Y., Quin W., Snider J., Schwartzenberg K. von. Adenosine kinase - contributions to adenylate and methyl recycling and cytokinin interconversion in Arabidopsis.  Plant Physiology. (2000);  124 1775-1785
• 41 Moffatt B. A., Stevens Y. Y., Allen M. S., Snider J. D., Pereira L. A., Todorova M. I., Summers P. S., Weretilnyk E. A., Martin-McCaffrey L., Wagner C.. Adenosine kinase deficiency is associated with developmental abnormalities and reduced transmethylation.  Plant Physiology. (2002);  128 812-821
• 42 Mok D. W. S., Mok M. C.. Cytokinin metabolism and action.  Annual Review of Plant Physiology and Plant Molecular Biology. (2001);  52 89-118
• 43 Morris R. O., Bilyeu K. D., Laskey J. G., Cheik N. N.. Isolation of a gene encoding for glycosylated cytokinin oxidase from maize.  Biochemical and Biophysical Research Communications. (1999);  255 328-333
• 44 Murai N.. Cytokinin biosynthesis in tRNA and cytokinin incorporation into plant RNA. Mok, D. and Mok, M., eds. Cytokinins, Chemistry, Activity and Function. Boca Raton; CRC Press (1994): 87-99
• 45 Nehlsen W.. A new method for examining induction of buds by cytokinin.  American Journal of Botany. (1979);  66 601
• 46 Perry K. C., Cove D.. Transfer RNA pool sizes and half lives in wild-type and cytokinin-overproducing strains of the moss Physcomitrella patens.  Physiologia Plantarum. (1986);  67 680-684
• 47 Reutter K., Atzorn R., Hadeler B., Schmülling T., Reski R.. Expression of the bacterial ipt gene in Physcomitrella rescues mutations in budding and in plastid division.  Planta. (1998);  206 196-203
• 48 Schaefer D. G.. A new moss genetics, targeted mutagenesis in Physcomitrella patens.  Annual Review of Plant Biology. (2002);  53 477-501
• 49 Schmülling T., Beinsberger S., De Greef J., Van Onckelen H., Spena A.. Construction of a heat inducible chimaeric gene to increase the cytokinin content in transgenic plant tissue.  FEBS Letters. (1989);  249 401-406
• 50 Schulz P.. Biochemische und molekulare Untersuchungen zum Cytokininstoffwechsel bei Physcomitrella patens (Hedw.) B.S.G. Dissertation, University of Hamburg, Germany. (2001)
• 51 Schulz P., Reski R., Maldiney R., Laloue M., Schwartzenberg K. von. Kinetics of cytokinin production and bud formation in Physcomitrella, analysis of wild type, a developmental mutant and two of its ipt transgenics.  Journal of Plant Physiology. (2000);  156 768-774
• 52 Schulz P., Hofmann A., Russo V., Hartmann E., Laloue M., Schwartzenberg K. von. Cytokinin overproducing ove mutants of Physcomitrella patens show increased riboside to base conversion.  Plant Physiology. (2001);  126 1224-1231
• 53 Schwartzenberg K. von, Doumas P., Jouanin L., Pilate G.. Enhancement of the endogenous cytokinin concentration in poplar by transformation with Agrobacterium T‐DNA gene ipt.  Tree Physiology. (1994);  14 27-35
• 54 Schwartzenberg K. von, Kruse S., Reski R., Moffatt B., Laloue M.. Cloning and characterisation of an adenosine kinase from Physcomitrella involved in cytokinin metabolism.  The Plant Journal. (1998);  13 249-257
• 55 Schwartzenberg K. von, Pethe C., Laloue M.. Cytokinin metabolism in Physcomitrella patens - differences and similarities to higher plants.  Plant Growth Regulation. (2003);  39 99-106
• 56 Skoog F., Hamzi H. Q., Szweykowska A. M., Leonard N. J., Carraway K. L., Fujii T., Helgeson J. P., Loeppky R. N.. Cytokinins, structure/activity relationships.  Phytochemistry. (1967);  6 1169-1192
• 57 Spichal L., Rakova N. Y., Riefler M., Mizuno T., Romanov G. A., Strnad M., Schmülling T.. Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3 differ in their ligand specificity in a bacterial assay.  Plant Cell Phyiology. (2004);  45 1299-1305
• 58 Stirk W. A., Ördög V., van Staden J.. Identification of the cytokinin isopentenyladenine in a strain of Arthronema africanum (Cyanobacteria).  Journal of Phycology. (1999);  35 89-92
• 59 Stirk W. A., Novák O., Strnad M., van Staden J.. Cytokinins in macroalgae.  Plant Growth Regulation. (2003);  41 13-24
• 60 Takei K., Sakakibara H., Sugiyama T.. Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthetic enzyme, in Arabidopsis thaliana.  Journal of Biological Chemistry. (2001);  276 26405-26410
• 61 Taller B.. Distribution, biosynthesis and function of cytokinins in tRNA. Mok, D. and Mok, M., eds. Cytokinins, Chemistry, Activity and Function. Boca Raton; CRC Press (1994): 101-112
• 62 Wang T., Cove D. J., Beutelmann P., Hartmann E.. Isopentenyladenine from mutants of the moss, Physcomitrella patens.  Phytochemistry. (1980);  19 1103-1105
• 63 Wang T. L., Beutelmann P., Cove D. J.. Cytokinin biosynthesis in mutants of the moss Physcomitrella patens.  Plant Physiology. (1981 a);  68 739-744
• 64 Wang T. L., Horgan R., Cove D.. Cytokinins from the moss Physcomitrella patens.  Plant Physiology. (1981 b);  68 735-738
• 65 Wang T. L., Futers T. S., Mc Geary F., Cove D. J.. Moss mutants and the analysis of cytokinin metabolism. Crozier, A. and Hillman, J. R., eds. The Biosynthesis and Metabolism of Plant Hormones. Cambridge; Cambridge University Press (1984): 135-164
• 66 Whitaker B. D., Kende H.. Bud formatin in Funaria hygrometrica: a comparison of the activities of three cytokinins with their ribosides.  Planta. (1974);  121 93-96
• 67 Yonekura-Sakakibara K., Kojima M., Yamaya T., Sakakibara H.. Molecular characterisation of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cytokinin.  Plant Physiology. (2004);  134 1654-1661

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