Analysis of Expressed Sequence Tags Derived from Developing Seed and Pollen Cones of Cryptomeria japonica

Abstract

We obtained 1210 expressed sequence tags (ESTs), representing 1173 transcripts, from two cDNA libraries, which derive from developing seed and pollen cones of sugi (Cryptomeria japonica). Among these 1173 transcripts, 807 showed notable similarity to known sequences, including those of genes expressed in developing flower tissues of other plant species, such as CONSTANS and the genes for MADS-domain proteins. This result indicates that, in spite of differences in morphology, the development of reproductive organs is regulated by a family of homologous transcription factors common to both gymnosperm and angiosperm species. The remaining 366 transcripts showed no significant similarity to any known sequences in public databases. Furthermore, we compared the 1173 transcripts to those derived from other tissues of C. japonica to investigate the possibility of tissue-specific transcripts, and found that 882 did not occur among ESTs derived from other tissues, such as the inner bark and seedlings. The ESTs developed during the present study most likely include tissue- and stage-specific transcripts, and these will contribute to a further understanding of the reproductive organ development of C. japonica.

Key words

Gymnosperm species - expressed sequence tags - reproductive organs.

References

• 1 Allona I., Quinn M., Shoop E., Swope K., St. Cyr S., Carlis J.. Analysis of xylem formation in pine by cDNA sequencing.  Proc. Natl. Acad. Sci. USA. (1998);  95 9693-9698
• 2 Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.  Nucleic Acids Res,. (1997);  25 3389-3402
• 3 Axelsson T., Lagercrantz U.. Rapid evolution of the family of CONSTANS LIKE genes in Plants.  Mol. Biol. Evol.. (2000);  17 1499-1507
• 4 Becker A., Kaufmann K., Freialdenhoven A., Vincent C., Li M. A., Saedler H., Theissen G.. A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes.  Mol Genet Genomics. (2002);  266 942-950
• 5 Dayhoff M. O.. Atlas of Protein Sequences and Structure, Vol. 5, supplement 3, 1978. Washington, DC; National Biomedical Research Foundation (1979): 121
• 6 Decrocq-Ferrant V., Went J. V., Bianchi M. W., Vries S. D., Kreis M.. Petunia hybrida homologues of shaggy/zeste-white 3 expressed in female and male reproductive organs.  Plant J.. (1995);  7 897-911
• 7 Don R. H., Cox P. T., Wainwright B. J., Baker K., Mattick J. S.. “Touch-down PCR” to circumvent spurious priming during gene amplification.  Nucl. Acids Res.. (1991);  19 4008
• 8 Dornelas M., Lammeren A. V., Kreis M.. Arabidopsis thaliana SHAGGY-related protein kinases (AtSK11 and 12) function in perianth and gynoecium development.  Plant J.. (2000);  21 419-429
• 9 Elliott R. C., Betzner A. S., Huttner E., Oakes M. P., Tucker W. Q., Gerentes D., Perez P., Smyth D. R.. AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth.  Plant Cell. (1996);  8 155-168
• 10 Endo M., Hakozaki H., Kokubun T., Masuko H., Takahata Y., Tsuchiya T., Higashitani A., Tabata S., Watanabe M.. Generation of 919 expressed sequence tags from immature flower buds and gene expression analysis using expressed sequence tags in the model plant Lotus japonicus. .  Genes Genet. Syst.. (2002);  77 277-282
• 11 Endo M., Kokubun T., Takahata Y., Higashitani A., Tabata S., Watanabe M.. Analysis of expressed sequence tags of flower buds in Lotus japonicus. .  DNA Research. (2000);  7 213-216
• 12 Felsenstein J.. PHYLIP Phylogeny Inference Package 3.5. The University of Washington; Department of Genetics (1993)
• 13 Fukui M., Futamura N., Mukai Y., Wang Y., Nagao A., Sinohara K.. Ancestral MADS box genes in sugi, Cryptomeria japonica D. Don (Taxodiaceae), homologous to the B function genes in angiosperm.  Plant Cell Physiol.. (2001);  42 566-575
• 14 Iwata H., Ujino-Ihara T., Yoshimaru K., Nagasaka K., Mukai Y., Tsumura Y.. Cleaved amplified polymorphic sequence markers in sugi, Cryptomeria japonica D. Don, and their location on a linkage map.  Theor. Appl. Genet.. (2001);  103 881-895
• 15 Jack T.. Relearning our ABCs, new twists on an old model.  Trends in Plant Science. (2001);  6 310-316
• 16 Lim C. O., Kim H. Y., Kim M. G., Lee S. I., Chung W. S., Park S. H., Hwang I. H., Cho M. J.. Expressed sequence tags of Chinese cabbage flower bud cDNA.  Plant Physiology. (1996);  111 577-588
• 17 Montag K., Salamini F., Thompson R. D.. ZEMa, a member of a novel group of MADS box genes, is alternatively spliced in maize endosperm.  Nucleic Acids Res. (1995);  23 2168-2177
• 18 Mouradov A., Cremer F., Coupland G.. Control of flowering time, interacting pathways as a basis for diversity.  Plant Cell. (2002);  14 S111-S130
• 19 Mouradov A., Glassick T., Hamdorf B., Murphy L., Fowler B., Marla S., Teasdale R. D.. NEEDLY, a Pinus radiata ortholog of FLORICAULA/LEAFY genes, expressed in both reproductive and vegetative meristems.  Proc. Natl. Acad. Sci.. (1998 a);  95 6537-6542
• 20 Mouradov A., Glassick T., Hamodorf B., Murphy L., Marla S., Yang Y., Teasdale R.. Family of MADS-box genes expressed early in male and female reproductive structures of Monterey pine.  Plant Physiol.. (1998 b);  117 55-62
• 21 Mouradov A., Hamdorf B., Teasdale R. D., Kim J. T., Winter K. U., Theissen G.. A DEF/GLO-like MADS-box gene from a gymnosperm, Pinus radiata, contains an ortholog of angiosperm B class floral homeotic genes.  Dev. Genet.. (1999);  25 245-252
• 22 Mukai Y., Suyama Y., Tsumura Y., Kawahara T., Yoshimaru H., Kondo T., Tomaru N., Kuramoto N., Murai M.. A linkage map for sugi (Cryptomeria japonica) based on RFLP, RAPD, and isozyme loci.  Theor. Appl. Genet.. (1995);  90 835-840
• 23 Mukai Y., Yamamoto N.. Extraction RNA from woody plants. Shimamoto, K. and Sasaki, T., eds. PCR Protocols for Plants. Tokyo, Japan; SHUJUNSHA Co. Ltd., in Japanese (1997): 60-62
• 24 Nam J., DePamphilis C. W., Ma H., Nei M.. Antiquity and evolution of the MADS-box gene family controlling flower development in Plants.  Mol. Biol. Evol.. (2003);  20 1435-1447
• 25 Nikaido A., Ujino T., Iwata H., Yoshimura K., Yoshimaru H., Suyama Y., Murai M., Nagasaka K., Tsumura Y.. AFLP and CAPS linkage maps of Cryptomeria japonica. .  Theor. Appl. Genet.. (2000);  100 825-831
• 26 Rutledge R., Regan S., Nicolas O., Fobert P., Cote C., Bosnich W., Kauffeldt C., Sunohara G., Seguin A., Stewart D.. Characterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis. .  Plant J.. (1998);  15 625-634
• 27 Saitou N., Nei M.. The neighbor-joining method, a new method for reconstructing phylogenetic trees.  Mol. Biol. Evol.. (1987);  4 406-425
• 28 Shindo S., Ito M., Ueda K., Kato M., Hasebe M.. Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants.  Evol. Dev.. (1999);  1 180-190
• 29 Sundström J., Carlsbecker A., Svensson M., Svenson M., Johanson U., Theissen G., Engstrom P.. MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms.  Dev. Genet.. (1999);  25 253-266
• 30 Sundström J., Engstrom P.. Conifer reproductive development involves B-type MADS-box genes with distinct and different activities in male organ primordia.  Plant J.. (2002);  31 161-169
• 31 Tandre K., Albert V. A., Sundas A., Engstrom P.. Conifer homologues to genes that control floral development in angiosperms.  Plant Mol. Biol.. (1995);  27 69-78
• 32 Tandre K., Svenson M., Svensson M., Engstrom P.. Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms.  Plant J.. (1998);  15 615-623
• 33 Theissen G., Becker A., Di Rosa A., Kanno A., Kim J. T., Munster T., Winter K. U., Saedler H.. A short history of MADS-box genes in plants.  Plant Mol. Biol.. (2000);  42 115-149
• 34 Theissen G., Kim J. T., Saedler H.. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes.  J. Mol. Evol.. (1996);  43 484-516
• 35 Tichtinsky G., Tavares R., Takvorian A., Schwebel-Dugue N., Twell D., Kreis M.. An evolutionary conserved group of plant GSK-3/shaggy-like protein kinase genes preferentially expressed in developing pollen.  Biochim. Biophys. Acta. (1998);  1442 261-273
• 36 Tsumura Y., Suyama Y., Yoshimura K., Shirato N., Mukai Y.. Sequence-tagged sites (STSs) of cDNA clones in Cryptomeria japonica and their evaluation as molecular markers in conifers.  Theor. Appl. Genet.. (1997);  94 764-772
• 37 Ujino-Ihara T., Matsumoto A., Iwata H., Yoshimura K., Tsumura Y.. Single-strand conformation polymorphism of sequence-tagged site markers based on partial sequences of cDNA clones in Cryptomeria japonica. .  Genes Genet. Syst.. (2002);  77 251-257
• 38 Ujino-Ihara T., Yoshimura K., Ugawa Y., Yoshimaru H., Nagasaka K., Tsumura Y.. Expression analysis of ESTs derived from the inner bark of Cryptomeria japonica. .  Plant Mol. Biol.. (2000);  43 451-457
• 39 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 J.. (2002);  31 457-475
• 40 Yano M., Katayose Y., Ashiraki M., Yamanouchi U., Monna L., Fuse T., Baba T., Yamamoto K., Umehara Y., Nagamura Y., Sasaki T.. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS.  Plant Cell. (2000);  12 2476-2483
• 41 Yanovsky M. J., Kay S. A.. Molecular basis of seasonal time measurement in Arabidopsis. .  Nature. (2002);  419 308-312

Section Editor: M. Koornneef