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Plant Biol (Stuttg) 2006; 8(3): 397-406
DOI: 10.1055/s-2006-923952
Review Article

Georg Thieme Verlag Stuttgart KG · New York

Moss Systems Biology en Route: Phytohormones in Physcomitrella Development

E. L. Decker1 , W. Frank1 , E. Sarnighausen1 , R. Reski1
  • 1Faculty of Biology, Plant Biotechnology, University of Freiburg, Schänzlestraße 1, 79104 Freiburg, Germany
Further Information

Publication History

Received: December 5, 2005

Accepted: January 31, 2006

Publication Date:
19 April 2006 (online)

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Abstract

The moss Physcomitrella patens has become a powerful model system in modern plant biology. Highly standardized cell culture techniques, as well as the necessary tools for computational biology, functional genomics and proteomics have been established. Large EST collections are available and the complete moss genome will be released soon. A simple body plan and the small number of different cell types in Physcomitrella facilitate the study of developmental processes. In the filamentous juvenile moss tissue, developmental decisions rely on the differentiation of single cells. Developmental steps are controlled by distinct phytohormones and integration of environmental signals. Especially the phytohormones auxin, cytokinin, and abscisic acid have distinct effects on early moss development. In this article, we review current knowledge about phytohormone influences on early moss development in an attempt to fully unravel the complex regulatory signal transduction networks underlying the developmental decisions of single plant cells in a holistic systems biology approach.

Key words

Bryophyte - cell cycle - homologous recombination - cell differentiation - auxin - cytokinin - ABA

References

  • 1 Ashton N. W., Grimsely N. H., Cove D. J.. Analysis of gametophytic development in the moss, Physcomitrella patens, using auxin and cytokinin resistant mutants.  Planta. (1979);  144 427-435
    CrossrefPubMedGoogle Scholar
  • 2 Bierfreund N. M., Reski R., Decker E. L.. Use of an inducible reporter gene system for the analysis of auxin distribution in the moss Physcomitrella patens.  Plant Cell Reports. (2003);  21 1143-1152
    CrossrefPubMedGoogle Scholar
  • 3 Bierfreund N. M., Tintelnot S., Reski R., Decker E. L.. Loss of GH3 function does not affect phytochrome-mediated development in a moss, Physcomitrella patens.  Journal of Plant Physiology. (2004);  161 823-835
    CrossrefPubMedGoogle Scholar
  • 4 Blilou I., Xu J., Wildwater M., Willemsen V., Paponov I., Friml J., Heidstra R., Aida M., Palme K., Scheres B.. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots.  Nature. (2005);  433 39-44
    CrossrefPubMedGoogle Scholar
  • 5 Bopp M., Atzorn R.. The morphogenetic system of the moss protonema.  Cryptogamic Botany. (1992);  3 3-10
    PubMedGoogle Scholar
  • 6 Chandler P. M., Robertson M.. Gene expression regulated by abscisic acid and its relation to stress tolerance.  Annual Review of Plant Physiology and Plant Molecular Biology. (1994);  45 113-141
    CrossrefPubMedGoogle Scholar
  • 7 Cove D. J., Knight C. D.. The moss Physcomitrella patens, a model system with potential for the study of plant reproduction.  Plant Cell. (1993);  5 1483-1488
    CrossrefPubMedGoogle Scholar
  • 8 Decker E. L., Reski R.. The moss bioreactor.  Current Opinion in Plant Biology. (2004);  7 166-170
    CrossrefPubMedGoogle Scholar
  • 9 den Boer B. G., Murray J. A.. Triggering the cell cycle in plants.  Trends in Cell Biology. (2000);  10 245-250
    CrossrefPubMedGoogle Scholar
  • 10 Ebel C., Mariconti L., Gruissem W.. Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte.  Nature. (2004);  429 776-780
    PubMedGoogle Scholar
  • 11 Egener T., Granado J., Guitton M. C., Hohe A., Holtorf H., Lucht J. M., Rensing S. A., Schlink K., Schulte J., Schween G., Zimmermann S., Duwenig E., Rak B., Reski R.. High frequency of phenotypic deviations in Physcomitrella patens plants transformed with a gene-disruption library.  BMC Plant Biology. (2002);  2 6
    CrossrefPubMedGoogle Scholar
  • 12 Ehness R., Ecker M., Godt D. E., Roitsch T.. Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation.  Plant Cell. (1997);  9 1825-1841
    CrossrefPubMedGoogle Scholar
  • 13 Frank W., Decker E. L., Reski R.. Molecular tools to study Physcomitrella patens.  Plant Biology. (2005 a);  7 220-227
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Frank W., Ratnadewi D., Reski R.. Physcomitrella patens is highly tolerant against drought, salt and osmotic stress.  Planta. (2005 b);  220 384-394
    CrossrefPubMedGoogle Scholar
  • 15 Friml J., Wisniewska J., Benkova E., Mendgen K., Palme K.. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis.  Nature. (2002);  415 806-809
    PubMedGoogle Scholar
  • 16 Grefen C., Harter K.. Plant two-component systems: principles, functions, complexity and cross talk.  Planta. (2004);  219 733-742
    PubMedGoogle Scholar
  • 71 Guilfoyle T. J.. Auxin-regulated genes and promoters. Hooykaas, P. P. J., Hall, M. A., and Libbenga, K. R., eds. Biochemistry and Molecular Biology of Plant Hormones. New York; Elsevier (1999): 423-459
    Google Scholar
  • 17 Gutierrez C.. The retinoblastoma pathway in plant cell cycle and development.  Current Opinion in Plant Biology. (1998);  1 492-497
    CrossrefPubMedGoogle Scholar
  • 18 Hagen G., Guilfoyle T.. Auxin-responsive gene expression: genes, promoters and regulatory factors.  Plant Molecular Biology. (2002);  49 373-385
    CrossrefPubMedGoogle Scholar
  • 19 Hagen G., Martin G., Li Y., Guilfoyle T. J.. Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants.  Plant Molecular Biology. (1991);  17 567-579
    CrossrefPubMedGoogle Scholar
  • 20 Heintz D., Wurtz V., High A. A., Van Dorsselaer A., Reski R., Sarnighausen E.. An efficient protocol for the identification of protein phosphorylation in a seedless plant, sensitive enough to detect members of signalling cascades.  Electrophoresis. (2004);  25 1149-1159
    CrossrefPubMedGoogle Scholar
  • 21 Hohe A., Rensing S. A., Mildner M., Lang D., Reski R.. Day length and temperature strongly influence sexual reproduction and expression of a novel MADS‐box gene in the moss Physcomitrella patens.  Plant Biology. (2002);  4 595-602
    Article in Thieme ConnectPubMedGoogle Scholar
  • 22 Hohe A., Reski R.. A tool for understanding homologous recombination in plants.  Plant Cell Reports. (2003);  21 1135-1142
    CrossrefPubMedGoogle Scholar
  • 23 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
  • 24 Hsieh H. L., Okamoto H., Wang M., Ang L. H., Matsui M., Goodman H., Deng X. W.. FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development.  Genes and Development. (2000);  14 1958-1970
    PubMedGoogle Scholar
  • 25 Huether C. M., Lienhart O., Baur A., Stemmer C., Gorr G., Reski R., Decker E. L.. Glyco-engineering of moss lacking plant-specific sugar residues.  Plant Biology. (2005);  7 292-299
    Article in Thieme ConnectPubMedGoogle Scholar
  • 26 Johri M. M., Desai S.. Auxin regulation of caulonema formation in moss protonema.  Nature (London), New Biology. (1973);  245 223-224
    PubMedGoogle Scholar
  • 27 Kamisugi Y., Cuming A. C.. The evolution of the abscisic acid-response in land plants: comparative analysis of group 1 LEA gene expression in moss and cereals.  Plant Molecular Biology. (2005);  59 723-737
    CrossrefPubMedGoogle Scholar
  • 28 Knight C. D., Sehgal A., Atwal K., Wallace J. C., Cove D. J., Coates D., Quatrano R. S., Bahadur S., Stockley P. G., Cuming A. C.. Molecular responses to abscisic acid and stress are conserved between moss and cereals.  Plant Cell. (1995);  7 499-506
    CrossrefPubMedGoogle Scholar
  • 29 Koprivova A., Stemmer C., Altmann F., Hoffmann A., Kopriva S., Gorr G., Reski R., Decker E. L.. Targeted knockouts of Physcomitrella lacking plant-specific immunogenic N-glycans.  Plant Biotechnology Journal. (2004);  2 517-523
    CrossrefPubMedGoogle Scholar
  • 30 Kroemer K., Reski R., Frank W.. Abiotic stress response in the moss Physcomitrella patens: evidence for an evolutionary alteration in signaling pathways in land plants.  Plant Cell Reports. (2004);  22 864-870
    CrossrefPubMedGoogle Scholar
  • 31 Kwak S. H., Lee S. H.. The requirements for Ca2+, protein phosphorylation, and dephosphorylation for ethylene signal transduction in Pisum sativum L.  Plant and Cell Physiology. (1997);  38 1142-1149
    PubMedGoogle Scholar
  • 32 Lang D., Eisinger J., Reski R., Rensing S. A.. Representation and high-quality annotation of the Physcomitrella patens transcriptome demonstrates a high proportion of proteins involved in metabolism in mosses.  Plant Biology. (2005);  7 238-250
    Article in Thieme ConnectPubMedGoogle Scholar
  • 33 Lorenz S., Tintelnot S., Reski R., Decker E. L.. Cyclin D-knockout uncouples developmental progression from sugar availability.  Plant Molecular Biology. (2003);  53 227-236
    CrossrefPubMedGoogle Scholar
  • 34 Minami A., Nagao M., Arakawa K., Fujikawa S., Takezawa D.. Abscisic acid-induced freezing tolerance in the moss Physcomitrella patens is accompanied by increased expression of stress-related genes.  Jornal of Plant Physiology. (2003);  160 475-483
    PubMedGoogle Scholar
  • 35 Minami A., Nagao M., Ikegami K., Koshiba T., Arakawa K., Fujikawa S., Takezawa D.. Cold acclimation in bryophytes: low-temperature-induced freezing tolerance in Physcomitrella patens is associated with increases in expression levels of stress-related genes but not with increase in level of endogenous abscisic acid.  Planta. (2005);  220 414-423
    CrossrefPubMedGoogle Scholar
  • 36 Nagao M., Minami A., Arakawa K., Fujikawa S., Takezawa D.. Rapid degradation of starch in chloroplasts and concomitant accumulation of soluble sugars associated with ABA-induced freezing tolerance in the moss Physcomitrella patens.  Journal of Plant Physiology. (2005);  162 169-180
    CrossrefPubMedGoogle Scholar
  • 37 Nakazawa M., Yabe N., Ichikawa T., Yamamoto Y. Y., Yoshizumi T., Hasunuma K., Matsui M.. DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length.  The Plant Journal. (2001);  25 213-221
    CrossrefPubMedGoogle Scholar
  • 38 Nishiyama T., Fujita T., Shin I. T., Seki M., Nishide H., Uchiyama I., Kamiya A., Carninci P., Hayashizaki Y., Shinozaki K., Kohara Y., Hasebe M.. Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution.  Proceedings of the National Acadamy of Sciences of the USA. (2003);  100 8007-8012
    CrossrefPubMedGoogle Scholar
  • 39 Oakenfull E. A., Riou-Khamlichi C., Murray J. A.. Plant D-type cyclins and the control of G1 progression.  Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences. (2002);  357 749-760
    CrossrefPubMedGoogle Scholar
  • 40 Olsson T., Thelander M., Ronne H.. A novel type of chloroplast stromal hexokinase is the major glucose-phosphorylating enzyme in the moss Physcomitrella patens.  Journal of Biological Chemistry. (2003);  278 44439-44447
    CrossrefPubMedGoogle Scholar
  • 41 Paponov I. A., Teale W. D., Trebar M., Blilou I., Palme K.. The PIN auxin efflux facilitators: evolutionary and functional perspectives.  Trends in Plant Sciences. (2005);  10 170-177
    PubMedGoogle Scholar
  • 42 Rensing S. A., Rombauts S., Van de Peer Y., Reski R.. Moss transcriptome and beyond.  Trends in Plant Sciences. (2002);  7 535-538
    CrossrefPubMedGoogle Scholar
  • 43 Repp A., Mikami K., Mittmann F., Hartmann E.. Phosphoinositide-specific phospholipase C is involved in cytokinin and gravity responses in the moss Physcomitrella patens.  The Plant Journal. (2004);  40 250-259
    CrossrefPubMedGoogle Scholar
  • 44 Reski R.. Development, genetics and molecular biology of mosses.  Botanica Acta. (1998);  111 1-15
    PubMedGoogle Scholar
  • 45 Reski R., Abel W. O.. Induction of budding on chloronemata and caulonemata of the moss, Physcomitrella patens, using isopentenyladenine.  Planta. (1985);  165 354-358
    CrossrefPubMedGoogle Scholar
  • 46 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
  • 47 Riou-Khamlichi C., Huntley R., Jacqmard A., Murray J. A.. Cytokinin activation of Arabidopsis cell division through a D-type cyclin.  Science. (1999);  283 1541-1544
    CrossrefPubMedGoogle Scholar
  • 48 Riou-Khamlichi C., Menges M., Healy J. M., Murray J. A.. Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression.  Molecular and Cellular Biology. (2000);  20 4513-4521
    CrossrefPubMedGoogle Scholar
  • 49 Rose S., Rubery P. H., Bopp M.. The mechanism of auxin uptake and accumulation in moss protonema.  Physiologia Plantarum. (1983);  58 52-56
    PubMedGoogle Scholar
  • 50 Sakakibara K., Nishiyama T., Sumikawa N., Kofuji R., Murata T., Hasebe M.. Involvement of auxin and a homeodomain-leucine zipper I gene in rhizoid development of the moss Physcomitrella patens.  Development. (2003);  130 4835-4846
    CrossrefPubMedGoogle Scholar
  • 51 Sarnighausen E., Wurtz V., Heintz D., Van Dorsselaer A., Reski R.. Mapping of the Physcomitrella patens proteome.  Phytochemistry. (2004);  65 1589-1607
    CrossrefPubMedGoogle Scholar
  • 52 Schaefer D. G.. A new moss genetics: targeted mutagenesis in Physcomitrella patens.  Annual Review of Plant Biology. (2002);  53 477-501
    PubMedGoogle Scholar
  • 53 Schipper O., Schaefer D., Reski R., Fleming A.. Expansins in the bryophyte Physcomitrella patens.  Plant Molecular Biology. (2002);  50 789-802
    CrossrefPubMedGoogle Scholar
  • 54 Schnepf E., Hrdina B., Lehne A.. Spore germination, development of the microtubule system and protonema cells morphogenesis in the moss, Funaria hygrometrica: effects of inhibitors and of growth substances.  Biochemie und Physiologie der Pflanzen. (1982);  177 461-482
    PubMedGoogle Scholar
  • 55 Schnepf E., Reinhard C.. Brachycytes in Funaria protonemate: induction by abscisic acid and fine structure.  Journal of Plant Physiology. (1997);  151 166-175
    PubMedGoogle Scholar
  • 56 Schulz P., Reski R., Maldiney R., Laloue M., v. Schwartzenberg K.. Kinetics of cytokinin production and bud formation in Physcomitrella: analysis of a wild type, a developmental mutant and two of its ipt transgenics.  Journal of Plant Physiology. (2000);  156 768-774
    PubMedGoogle Scholar
  • 57 Schween G., Egener T., Fritzowsky D., Granado J., Guitton M. C., Hartmann N., Hohe A., Holtorf H., Lang D., Lucht J. M., Reinhard C., Rensing S. A., Schlink K., Schulte J., Reski R.. Large-scale analysis of 73 329 Physcomitrella plants transformed with different gene disruption libraries: production parameters and mutant phenotypes.  Plant Biology. (2005);  7 228-237
    Article in Thieme ConnectPubMedGoogle Scholar
  • 58 Schween G., Hohe A., Koprivova A., Reski R.. Effects of nutrients, cell density and culture techniques on protoplast regeneration and early protonema development in a moss, Physcomitrella patens.  Journal of Plant Physiology. (2003);  160 209-212
    PubMedGoogle Scholar
  • 59 Staswick P. E., Serban B., Rowe M., Tiryaki I., Maldonado M. T., Maldonado M. C., Suza W.. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid.  Plant Cell. (2005);  17 616-627
    CrossrefPubMedGoogle Scholar
  • 60 Staswick P. E., Tiryaki I., Rowe M. L.. Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation.  Plant Cell. (2002);  14 1405-1415
    CrossrefPubMedGoogle Scholar
  • 61 Strepp R., Scholz S., Kruse S., Speth V., Reski R.. Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin.  Proceedings of the National Academy of Sciences of the USA. (1998);  95 4368-4373
    CrossrefPubMedGoogle Scholar
  • 62 Takase T., Nakazawa M., Ishikawa A., Kawashima M., Ichikawa T., Takahashi N., Shimada H., Manabe K., Matsui M.. ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation.  The Plant Journal. (2004);  37 471-483
    CrossrefPubMedGoogle Scholar
  • 63 Takase T., Nakazawa M., Ishikawa A., Manabe K., Matsui M.. DFL2, a new member of the Arabidopsis GH3 gene family, is involved in red light-specific hypocotyl elongation.  Plant and Cell Physiology. (2003);  44 1071-1080
    CrossrefPubMedGoogle Scholar
  • 64 Tanaka S., Mochizuki N., Nagatani A.. Expression of the AtGH3a gene, an Arabidopsis homologue of the soybean GH3 gene, is regulated by phytochrome B.  Plant and Cell Physiology. (2002);  43 281-289
    CrossrefPubMedGoogle Scholar
  • 65 Thelander M., Olsson T., Ronne H.. Effect of the energy supply on filamentous growth and development in Physcomitrella patens.  Journal of Experimental Botany. (2005);  56 653-662
    CrossrefPubMedGoogle Scholar
  • 66 Vandepoele K., Raes J., De Veylder L., Rouze P., Rombauts S., Inze D.. Genome-wide analysis of core cell cycle genes in Arabidopsis.  Plant Cell. (2002);  14 903-916
    CrossrefPubMedGoogle Scholar
  • 67 von Schwartzenberg K., Kruse S., Reski R., Moffatt B., Laloue M.. Cloning and characterization of an adenosine kinase from Physcomitrella involved in cytokinin metabolism.  The Plant Journal. (1998);  13 249-257
    CrossrefPubMedGoogle Scholar
  • 68 Woodward A. W., Bartel B.. Auxin: regulation, action, and interaction.  Annals of Botany (London). (2005);  95 707-735
    CrossrefPubMedGoogle Scholar
  • 69 Wu G., Truksa M., Datla N., Vrinten P., Bauer J., Zank T., Cirpus P., Heinz E., Qiu X.. Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants.  Nature Biotechnology. (2005);  23 1013-1017
    CrossrefPubMedGoogle Scholar
  • 70 Yu L. R., Conrads T. P., Uo T., Kinoshita Y., Morrison R. S., Lucas D. A., Chan K. C., Blonder J., Issaq H. J., Veenstra T. D.. Global analysis of the cortical neuron proteome.  Molecular and Cellular Proteomics. (2004);  3 896-907
    PubMedGoogle Scholar

R. Reski

Faculty of Biology
Plant Biotechnology
University of Freiburg

Schänzlestraße 1

79104 Freiburg

Germany

Email: ralf.reski@biologie.uni-freiburg.de

Editor: H. Rennenberg

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