Download PDF
Plant Biol (Stuttg) 2005; 7(3): 307-314
DOI: 10.1055/s-2005-865640
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Isolation and Characterization of New MIKC*-Type MADS-Box Genes from the Moss Physcomitrella patens

M. Riese[*] 1 , W. Faigl[*] 1 , V. Quodt1 , W. Verelst1 , A. Matthes1 , H. Saedler1 , T. Münster1
  • 1Abteilung Molekulare Pflanzengenetik, Max-Planck-Institut für Züchtungsforschung, Carl-von-Linné-Weg 10, 50829 Köln, Germany
Further Information

Publication History

Received: January 17, 2005

Accepted: April 4, 2005

Publication Date:
23 May 2005 (online)

   Permissions and Reprints

Abstract

MADS-box genes encode for a large family of transcription-regulating proteins, which were isolated from all groups of eukaryotic organisms. The plant-specific MIKC-type MADS-box genes have been intensively analyzed for their roles in controlling developmental processes. Well-known are the MADS-box genes acting as homeotic selector genes in the differentiation of whorls of floral organs in seed plants. The MADS-box gene family has also been studied in non-flowering plants, such as lycophytes, pteridophytes, and bryophytes. The analysis of MADS-box genes in the moss Physcomitrella patens led to the identification of a new class of MIKC-type genes, designated as MIKC*-type genes. The MIKC*-type genes possess a number of structural features which clearly distinguish them from the already known MIKC-type genes. Recently, orthologues of the Physcomitrella MIKC*-type genes were found in Arabidopsis thaliana, demonstrating the conservation of these genes in tracheophytes. Here, we report the isolation of two new MIKC*-type MADS-box genes from Physcomitrella. Structural features and expression patterns of these genes were analyzed. The contribution of our findings to a better understanding of the evolution of MIKC*-type genes in land plants is discussed.

Key words

Physcomitrella patens - moss - MADS-box gene - MIKC*-type - evolution.

Literature

  • 1 Cho S., Jang S., Chae S., Chung K. M., Moon Y.-H., An G., Jang S. K.. Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain.  Plant Molecular Biology. (1999);  40 419-429
    CrossrefPubMedSearch in Google Scholar
  • 2 Coen E. S., Meyerowitz E. M.. The war of the whorls: genetic interactions controlling flower development.  Nature. (1991);  353 31-37
    CrossrefPubMedSearch in Google Scholar
  • 3 Davies B., Schwarz-Sommer Z.. Control of floral organ identity by homeotic MADS-box transcription factors. Nover, L., ed. Results and Problems in Cell Differentiation, Vol. 20. Plant Promoters and Transcription Factors. Berlin; Springer (1994): 235-258
    Search in Google Scholar
  • 4 Doyle J. J., Doyle J. L.. A rapid isolation procedure for small quantities of fresh leaf tissue.  Phytochemical Bulletin. (1987);  19 11
    PubMedSearch in Google Scholar
  • 5 Egea-Cortines M., Saedler H., Sommer H.. Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. .  EMBO Journal. (1999);  18 5370-5379
    CrossrefPubMedSearch in Google Scholar
  • 6 Hasebe M., Wen C.-K., Kato M., Banks J. A.. Characterization of MADS homeotic genes in the fern Ceratopteris richardii. .  Proceedings of the National Academy of Sciences of the USA. (1998);  95 6222-6227
    CrossrefPubMedSearch in Google Scholar
  • 7 He Y., Doyle M. R., Amasino R. M.. PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization responsive, winter-annual habit in Arabidopsis. .  Genes and Development. (2004);  18 2774-2784
    CrossrefPubMedSearch in Google Scholar
  • 8 Hennig L., Gruissem W., Grossniklaus U., Köhler C.. Transcriptional programs of early reproductive stages in Arabidopsis. .  Plant Physiology. (2004);  135 1765-1775
    CrossrefPubMedSearch in Google Scholar
  • 9 Henschel K., Kofuji R., Hasebe M., Saedler H., Münster T., Theißen G.. Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. .  Molecular Biology and Evolution. (2002);  19 801-814
    PubMedSearch in Google Scholar
  • 10 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
    Thieme ConnectPubMedSearch in Google Scholar
  • 11 Honma T., Goto K.. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs.  Nature. (2001);  409 525-529
    CrossrefPubMedSearch in Google Scholar
  • 12 Kofuji R., Sumikawa N., Yamasaki M., Kondo K., Ueda K., Ito M., Hasebe M.. Evolution and divergence of the MADS-Box gene family based on genome-wide expression analyses.  Molecular Biology and Evolution. (2003);  20 1963-1977
    CrossrefPubMedSearch in Google Scholar
  • 13 Krogan N. T., Ashton N. W.. Ancestry of plant MADS-box genes revealed by bryophyte (Physcomitrella patens) homologues.  New Phytologist. (2000);  147 505-517
    CrossrefPubMedSearch in Google Scholar
  • 14 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
    Thieme ConnectPubMedSearch in Google Scholar
  • 15 Logemann J., Schell J., Willmitzer L.. Improved methods for the isolation of RNA from plant tissues.  Analytical Biochemistry. (1987);  163 16-20
    CrossrefPubMedSearch in Google Scholar
  • 16 Münster T., Pahnke J., Di Rosa A., Kim J. T., Martin W., Saedler H., Theißen G.. Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants.  Proceedings of the National Academy of Sciences of the USA. (1997);  94 2415-2420
    CrossrefPubMedSearch in Google Scholar
  • 17 Münster T., Faigl W., Saedler H., Theißen G.. Evolutionary aspects of MADSbox genes in the eusporangiate fern Ophioglossum. .  Plant Biology. (2002);  4 474-483
    Thieme ConnectPubMedSearch in Google Scholar
  • 18 Nishiyama T., Fujita T., Shin-I. T., Seki M., Nishide H., Uchiyama I., Kamiya A., Carnici 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 Academy of Sciences of the USA. (2003);  100 8007-8012
    CrossrefPubMedSearch in Google Scholar
  • 19 Pařenicová L., de Folter S., Kieffer M., Horner D. S., Favalli C., Busscher J., Cook H. E., Ingram R. M., Kater M. M., Davies B., Angenent G. C., Colombo L.. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: New openings to the MADS World.  Plant Cell. (2003);  15 1538-1551
    CrossrefPubMedSearch in Google Scholar
  • 20 Riechmann J. L., Meyerowitz E. M.. MADS domain proteins in plant development.  Journal of Biological Chemistry. (1997);  378 1079-1101
    PubMedSearch in Google Scholar
  • 21 Sambrook J., Fritsch E. F., Maniatis T.. Molecular Cloning: A Laboratory Manual, 2nd ed. New York, Cold Spring Harbor; Cold Spring Harbor Laboratory Press (1989)
    Search in Google Scholar
  • 22 Schaefer D. G., Zrӱd. J.-P.. Efficient gene targeting in the moss Physcomitrella patens. .  Plant Journal. (1997);  11 1195-1206
    CrossrefPubMedSearch in Google Scholar
  • 23 Schaefer D. G.. Gene targeting in Physcomitrella patens. .  Current Opinion in Plant Biology. (2001);  4 143-150
    CrossrefPubMedSearch in Google Scholar
  • 24 Schaefer D. G.. A new moss genetics: targeted mutagenesis in Physcomitrella patens. .  Annual Review of Plant Physiology. (2002);  53 477-501
    PubMedSearch in Google Scholar
  • 25 Schwarz-Sommer Z., Huijser P., Nacken W., Saedler H., Sommer H.. Genetic control of flower development by homeotic genes in Antirrhinum majus. .  Science. (1990);  250 931-936
    PubMedSearch in Google Scholar
  • 26 Schwarz-Sommer Z., Hue I., Huijser P., Flor P. J., Hansen R., Tetens F., Lönnig W. E., Saedler H., Sommer H.. Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development.  EMBO Journal. (1992);  11 251-263
    PubMedSearch in Google Scholar
  • 27 Shore P., Sharrocks D.. The MADS-box family of transcription factors.  European Journal of Biochemistry. (1995);  229 1-13
    CrossrefPubMedSearch in Google Scholar
  • 28 Soltis D. E., Soltis P. S., Albert V. A., Oppenheimer D. G., dePamphilis C. W., Ma H., Frohlich M., Theißen G.. Missing links: the architecture of flower and floral diversification.  Trends in Plant Science. (2002);  7 22-31
    CrossrefPubMedSearch in Google Scholar
  • 29 Sundström J., Engström P.. Conifer reproductive development involves B-type MADS-box genes with distinct and different activities in male organ primordia.  Plant Journal. (2002);  31 161-169
    CrossrefPubMedSearch in Google Scholar
  • 30 Svensson M. E., Engström P.. Closely related MADS-box genes in club moss (Lycopodium) show broad expression patterns and are structurally similar to, but phylogenetically distinct from, typical seed plant MADS-box genes.  New Phytologist. (2002);  154 439-450
    CrossrefPubMedSearch in Google Scholar
  • 35 Tanabe Y., Hasebe M., Sekimoto H., Nishiyama T., Kitani M., Henschel K., Münster T., Theißen G., Nozaki H., Ito M.. Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes.  Proceedings of the National Academy of Sciences of the USA. (2005);  102 2436-2441
    CrossrefPubMedSearch in Google Scholar
  • 31 The Arabidopsis Genome Initiative . Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. .  Nature. (2000);  408 796-815
    CrossrefPubMedSearch in Google Scholar
  • 32 Theißen G., Becker A., Di Rosa A., Kanno A., Kim J. T., Münster T., Winter K.-U., Saedler H.. A short history of MADS-box genes in plants.  Plant Molecular Biology. (2000);  42 115-149
    CrossrefPubMedSearch in Google Scholar
  • 33 Theißen G., Saedler H.. Floral quartets.  Nature. (2001);  409 469-471
    CrossrefPubMedSearch in Google Scholar
  • 34 Winter K.-U., Saedler H., Theißen G.. On the origin of class B floral homeotic genes: functional substitution and dominant inhibition in Arabidopsis by expression of an orthologue from the gymnosperm Gnetum. .  Plant Journal. (2002);  31 457-475
    CrossrefPubMedSearch in Google Scholar

1 * These authors contributed equally to this work

T. Münster

Abteilung Molekulare Pflanzengenetik
Max-Planck-Institut für Züchtungsforschung

Carl-von-Linné-Weg 10

50829 Köln

Germany

Email: muenster@mpiz-koeln.mpg.de

Guest Editor: R. Reski