Download PDF
Plant Biol (Stuttg) 2006; 8(3): 382-388
DOI: 10.1055/s-2006-923962
Review Article

Georg Thieme Verlag Stuttgart KG · New York

Moss Biology and Phytohormones - Cytokinins in Physcomitrella

K. von Schwartzenberg1
  • 1Biozentrum Klein Flottbek und Botanischer Garten, Universität Hamburg, Ohnhorststraße 18, 22609 Hamburg, Germany
Further Information

Publication History

Received: November 18, 2005

Accepted: February 1, 2006

Publication Date:
19 April 2006 (online)

   Permissions and Reprints

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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 4 Barnes M. F., Tien C. L., Gray J. S.. Biosynthesis of cytokinins by potato cell cultures.  Phytochemistry. (1980);  19 409-412
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 6 Bauer L.. Isolierung und Testung einer kinetinartigen Substanz aus Kalluszellen von Laubmoossporophyten.  Zeitschrift für Pflanzenphysiologie. (1966);  54 241-253
    PubMedGoogle Scholar
  • 7 Beutelmann P.. Untersuchungen zur Biosynthese eines Cytokinins in Calluszellen von Laubmoossporophyten.  Planta. (1973);  112 181-189
    CrossrefPubMedGoogle Scholar
  • 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
    Google Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    Google Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Google Scholar
  • 13 Chen C.-M.. Cytokinin biosynthesis and interconversion.  Physiologia Plantarum. (1997);  101 665-673
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    Google Scholar
  • 16 Edwards C. A., Armstrong D. J.. Cytokinin-active ribonucleosides in Phaseolus RNA.  Plant Physiology. (1981);  67 1185-1189
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 18 Ferreira F. J., Kieber J. J.. Cytokinin signaling.  Current Opinion in Plant Biology. (2005);  8 518-525
    CrossrefPubMedGoogle Scholar
  • 19 Frank W., Decker E. L., Reski R.. Molecular tools to study Physcomitrella patens.  Plant Biology. (2005);  7 220-227
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 22 Gorton B. S., Eakin R. E.. Development of the gametophyte in the moss Tortella caespitosa.  Botanical Gazette. (1957);  119 31-38
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 24 Haberer G., Kieber J. J.. Cytokinins. New insights into a classic phytohormone.  Plant Physiology. (2002);  128 354-362
    CrossrefPubMedGoogle Scholar
  • 25 Hahn H., Bopp M.. A cytokinin test with high specifity.  Planta. (1968);  83 115-118
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 28 Jahn H.. Der Einfluss von Kinetin auf die Anlage der Stämmchen von Funaria hygrometrica Sibth.  Flora. (1964);  154 568
    PubMedGoogle Scholar
  • 29 Johri M. M.. Possible origin of hormonal regulation in green plants.  Proceedings of the Indian National Science Academy. (2004);  70 335-365
    PubMedGoogle Scholar
  • 30 Kakimoto T.. Identification of plant cytokinin biosynthetic enzymes as dimethyl diphosphate, ATP/ADP isopentenyltransferases.  Plant and Cell Physiology. (2001);  42 677-685
    CrossrefPubMedGoogle Scholar
  • 31 Kakimoto T.. Biosynthesis of cytokinins.  Journal of Plant Research. (2003);  116 233-239
    CrossrefPubMedGoogle Scholar
  • 32 Kaminek M., Motyka V., Vankova R.. Regulation of cytokinin content in plant cells.  Physiologia Plantarum. (1997);  101 689-700
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 34 Klämbt D., Holtz J., Helbach M., Maaß H.. Die Biogenese der Cytokinine.  Berichte der Deutschen Botanischen Gesellschaft. (1984);  97 57-65
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    Google Scholar
  • 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
    Google Scholar
  • 38 Letham D. S.. Zeatin, a factor inducing cell division from Zea mays.  Life Science. (1963);  8 569-573
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Google Scholar
  • 45 Nehlsen W.. A new method for examining induction of buds by cytokinin.  American Journal of Botany. (1979);  66 601
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 48 Schaefer D. G.. A new moss genetics, targeted mutagenesis in Physcomitrella patens.  Annual Review of Plant Biology. (2002);  53 477-501
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 50 Schulz P.. Biochemische und molekulare Untersuchungen zum Cytokininstoffwechsel bei Physcomitrella patens (Hedw.) B.S.G. Dissertation, University of Hamburg, Germany. (2001)
    Google Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 59 Stirk W. A., Novák O., Strnad M., van Staden J.. Cytokinins in macroalgae.  Plant Growth Regulation. (2003);  41 13-24
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Google Scholar
  • 62 Wang T., Cove D. J., Beutelmann P., Hartmann E.. Isopentenyladenine from mutants of the moss, Physcomitrella patens.  Phytochemistry. (1980);  19 1103-1105
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 64 Wang T. L., Horgan R., Cove D.. Cytokinins from the moss Physcomitrella patens.  Plant Physiology. (1981 b);  68 735-738
    PubMedGoogle Scholar
  • 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
    Google Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar

K. von Schwartzenberg

Biozentrum Klein Flottbek und Botanischer Garten
Universität Hamburg

Ohnhorststraße 18

22609 Hamburg

Germany

Email: kvschwartzenberg@iangbot.uni-hamburg.de

Guest Editor: R. Reski