Skip to main content
SpringerLink
Log in

Two S-adenosylmethionine synthetase-encoding genes differentially expressed during adventitious root development in Pinus contorta

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Two S-adenosylmethionine synthetase (SAMS) cDNAs, PcSAMS1 and PcSAMS2, have been identified in Pinus contorta. We found that the two genes are differentially expressed during root development. Thus, PcSAMS1 is preferentially expressed in roots and exhibits a specific expression pattern in the meristem at the onset of adventitious root development, whereas PcSAMS2 is expressed in roots as well as in shoots and is down-regulated during adventitious root formation. The expression of the two SAMS genes is different from the SAMS activity levels during adventitious root formation. We conclude that other SAMS genes that remain to be characterized may contribute to the observed SAMS activity, or that the activities of PcSAMS1 and PcSAMS2 are affected by post-transcriptional regulation. The deduced amino acid sequences of PcSAMS1 and PcSAMS2 are highly divergent, suggesting different functional roles. However, both carry the two perfectly conserved motifs that are common to all plant SAMS. At the protein level, PcSAMS2 shares about 90% identity to other isolated eukaryotic SAMS, while PcSAMS1 shares less than 50% identity with other plant SAMS. In a phylogenetic comparison, PcSAMS1 seems to have diverged significantly from all other SAMS genes. Nevertheless, PcSAMS1 was able to complement a Saccharomyces cerevisiae sam1 sam2 double mutant, indicating that it encodes a functional SAMS enzyme.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Altamura, M.M., Torrigiani, P., Capitani, F., Scaramagli, S. and Bagni, N. 1991. De novo root formation in tobacco thin layers is affected by inhibition of polyamine biosynthesis. J. Exp. Bot. 42: 1575–1582.

    Google Scholar 

  • Boerjan, W., Bauw, G., Van Montagu, M. and Inzé, D. 1994. Distinct phenotypes generated by overexpression and suppression of S-adenosyl-L-methionine synthetase reveal developmental patterns of gene silencing in tobacco. Plant Cell 6: 1401–1414.

    Article  PubMed  Google Scholar 

  • Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Chem. 72: 248–254.

    Google Scholar 

  • Cantoni, G.L. 1953. S-adenosylmethionine: a new intermediate formed enzymatically from L-methionine and adenosinetriphosphate. J. Biol. Chem. 204: 403–416.

    PubMed  Google Scholar 

  • Chang, S., Puryear, J. and Cairney, J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11: 113–116.

    Google Scholar 

  • Chang, S., Puryear, J.D., Dias, D.L., Funkhouser, E.A., Newton, R.J. and Cairney, J. 1996. Gene expression under water deficit in loblolly pine (Pinus taeda): isolation and characterisation of cDNA clones. Physiol. Plant. 97: 139–148.

    Google Scholar 

  • Cheng, J.-C., Seeley, K.A. and Sung, Z. 1995. RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol. 107: 365–376.

    PubMed  Google Scholar 

  • Chiang, P.K., Gordon, R.K., Tal, J., Zeng, G.C., Doctor, B.P., Pardhasaradhi, K. and McCann, P.P. 1996. S-adenosylmethionine and methylation. FASEB J. 10: 471–480.

    PubMed  Google Scholar 

  • Dekeyser, R.A., Claes, B., De Rycke, R., Habets, M., Van Montagu, M. and Caplan, A. 1990. Transient gene expression in intact and organized rice tissues. Plant Cell 2: 591–602.

    Article  PubMed  Google Scholar 

  • Eliasson, L. 1978. Effects of nutrients and light on growth and root formation on Pisum sativum cuttings. Physiol. Plant. 43: 13–18.

    Google Scholar 

  • Espartero, J., Pintor-Toro, J.A. and Pardo, J.M. 1994. Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol. Biol. 25: 217–227.

    Google Scholar 

  • Galston, A.W.G. and Kaur-Sawhney, R. 1995. Polyamines as endogenous growth regulators. In: P.J. Davies (Ed.) Plant Hormones, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. C1: 158–178.

    Google Scholar 

  • Gómez-Gómez, L. and Carrasco, P. 1998. Differential expression of the S-adenosyl-L-methionine synthetase during pea development. Plant Physiol. 117: 397–405.

    PubMed  Google Scholar 

  • Grönroos, R. and von Arnold, S. 1987. Initiation of roots on hypocotyl cuttings of Pinus contorta in vitro. Physiol. Plant. 69: 227–236.

    Google Scholar 

  • Horikawa, S., Sasuga, J., Shimizu, K., Ozasa, H. and Tsukada, K. 1990. Molecular cloning and nucleotide sequence of cDNA encoding the rat kidney S-adenosylmethionine synthetase. J. Biol. Chem. 265: 13683–13686.

    PubMed  Google Scholar 

  • Ingestad, T. and Lund, A.-B. 1979. Nitrogen stress in birch Betula verrucosa seedlings. I. Growth technique and growth. Physiol. Plant. 45: 137–148.

    Google Scholar 

  • Keller, B. and Lamb, C.J. 1989. Specific expression of a novel cell wall hydroxyproline-rich glycoprotein in lateral root initiation. Genes Dev. 3: 1639–1646.

    PubMed  Google Scholar 

  • Kinlaw, C.S. and Neale, D.B. 1997. Complex gene families in pine genomes. Trends Plant Sci. 2: 356–359.

    Google Scholar 

  • Kotb, M. and Geller, A.M. 1993. Methionine adenosyltransferase: structure and function. Pharmaceut. Theory 59: 125–143.

    Google Scholar 

  • Kotb, M., Mudd, S.H., Mato, J.M., Geller, A.M., Kredich, N.M., Chou, J.Y. and Cantoni, G.L. 1997. Consensus nomenclature for the mammalian methionine adenosyltransferase genes and gene products. Trends Genet. 13: 51–52.

    Google Scholar 

  • Kumar, A., Altabella, T., Taylor, M. and Tiburcio, A.F. 1997. Recent advances in polyamine research. Trends Plant Sci. 2: 124–130.

    Google Scholar 

  • Kumar, A., Taylor, M.A., Mad Arif, S.A. and Davies, H.V. 1996. Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: antisense plants display abnormal phenotypes. Plant J. 9: 147–158.

    Google Scholar 

  • Kvarnheden, A., Alberts, V.A. and Engström, P. 1998. Molecular evolution of cdc2 pseudogenes in spruce (Picea). Plant Mol. Biol. 36: 767–774.

    Google Scholar 

  • Laskowski, M.J., Williams, M.E., Nusbaum, H.C. and Sussex, I.M. 1995. Formation of lateral root meristems is a two-stage process. Development 121: 3303–3310.

    PubMed  Google Scholar 

  • Lindroth, A. 2000. Gene expression during adventitious root development in Pinus contorta. Ph.D. dissertation, Silvestria 131, Swedish University of Agricultural Sciences, Uppsala, Sweden.

    Google Scholar 

  • Lindroth, A.M., Grönroos, R., Clapham, D., Svensson, J. and von Arnold, S. 1999. Ubiquitous and tissue-specific gus expression in transgenic roots conferred by six different promoters in one coniferous and three angiosperm species. Plant Cell Rep. 18: 820–828.

    Google Scholar 

  • Lindroth, A.M., Kvarnheden, A. and von Arnold, S. 2001. Isolation of a PSTAIRE CDC2 cDNA from Pinus contorta and its expression during adventitious root development. Plant Phys. Biochem., 39: 107–114.

    Google Scholar 

  • Luo, G., An, G. and Reen, W. 1994. A PCR differential screening method for rapid isolation of clones from a cDNA library. Biotechniques 16: 672–675.

    Google Scholar 

  • Masucci, J.D. and Schiefelbein, J.W. 1994. The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin-and ethylene-associated process. Plant Physiol. 106: 1335–1346.

    PubMed  Google Scholar 

  • Mathur, M., Saluja, D. and Sachar, R.C. 1991. Posttranscriptional regulation of S-adenosylmethionine synthetase from its stored messenger-RNA in germinated wheat embryos. Biochim. Biophys. Acta 1078: 161–170.

    PubMed  Google Scholar 

  • Mayne, M.B., Coleman, J.R. and Blumwald, E. 1996. Differential expression during drought conditioning of a root-specific S-adenosylmethionine synthetase from jack pine (Pinus banksiana Lamb.) seedlings. Plant Cell Envir. 19: 958–966

    Google Scholar 

  • McKeon, T.A., Fernández-Maculet, J.C. and Yang, S-F. 1995. Biosynthesis and metabolism of ethylene. In: P.J. Davies (Ed.) Plant Hormones, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. B4: 118–139.

    Google Scholar 

  • Nickel, L.G. 1991. Use of growth regulating chemicals. In: A.S. Raghavendra (Ed.) Physiology of Trees, Wiley Interscience, New York, pp. 467–487.

    Google Scholar 

  • Pajares, M.A., Corrales, F.J., Ochoa, P. and Mato, J.M. 1991. The role of cysteine-150 in the structure and activity of rat liver S-adenosylmethionine synthetase. Biochem J. 274: 225–229.

    PubMed  Google Scholar 

  • Peleman, J., Boerjan, W., Engler, G., Seurinck, J., Botterman, J., Alliotte, T., Van Montagu, M. and Inzé, D. 1989a. Strong cellular preference in the expression of a housekeeping gene in Arabidopsis thaliana encoding S-adenosylmethionine synthetase. Plant Cell 1: 81–93.

    PubMed  Google Scholar 

  • Peleman, J., Saito, K., Cottyn, B., Engler, G., Seurinck, J., Van Montagu, M. and Inzé, D. 1989b. Structure and expression analyses of the S-adenosylmethionine synthetase gene family in Arabidopsis thaliana. Gene 84: 359–369.

    PubMed  Google Scholar 

  • Reed, K.R. 1991. Nucleic acid hybridizations with positive charge-modified nylon membrane. In: J.W. Dale and P.G. Sanders (Eds.) Methods in Gene Technology, Vol. 1, JAI Press, London, pp. 127–160.

    Google Scholar 

  • Ronne, H., Carlberg, M., Hu, G.-Z. and Nehlin, J.O. 1991. Protein phosphatase 2A in Saccharomyces cerevisiae: eggects on cell growth and bud morphogenesis. Mol. Cell. Biol. 11: 4876–4884.

    Google Scholar 

  • Rost, T.L. and Bryant, J.A. 1996. Root organization and gene expression patterns. J. Exp. Bot. 47: 1613–1628.

    Google Scholar 

  • Rowland, L.J. and Nguyen, B. 1993. Use of polyethylene glycol for purification of DNA from leaf tissue of woody plants. Biotechniques 14: 735–736.

    Google Scholar 

  • Schröder, G., Eichel, J., Breinig, S. and Schröder, J. 1997. Three differentially expressed S-adenosylmethionine synthetases from Catharanthus roseus: molecular and functional characterization. Plant Mol. Biol. 3: 211–222.

    Google Scholar 

  • Smith, D.L. and Fedoroff, N.V. 1995. LRP1, a gene expressed in lateral and adventitious root primordia of Arabidopsis. Plant Cell 7: 735–745.

    PubMed  Google Scholar 

  • Sundås, A., Tandre, K., Holmstedt, E. and Engström, P. 1992. Differential gene expression during germination and after the induction of adventitious bud formation in Norway spruce embryos. Plant Mol. Biol. 18: 713–724.

    Google Scholar 

  • Takusagawa, F., Kamitori, S. and Markham, G.D. 1996. Structure and function of S-adenosylmethionine synthetase: crystal structure of S-adenosylmethionine synthetase with ADP, BrADP, and PP ί at 2.8 Å resolution. Biochemistry USA 35: 2586–2596.

    Google Scholar 

  • Thomas, D., Rothstein, R., Rosenberg, N. and Surdin-Kerjan, Y. 1988. Sam2 encodes the second methionine S-adenosyl transferase in Saccharamyces cerevisiae: physiology and regulation of both enzymes. Mol. Cell. Biol. 8: 5132–5139.

    Google Scholar 

  • Vera, P., Lamb, C., Doerner, P.W. 1994. Cell-cycle regulation of hydroxyproline-rich glycoprotein HRGPnt3 gene expression during the initiation of lateral root meristems. Plant J. 6: 717–727.

    Google Scholar 

  • Visser, E.J.W., Cohen, J.D., Barendse, G.W.M., Blom, C.W.P.M. and Voesenek, L.A.C.J. 1996. An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm. Plant Physiol. 112: 1687–1692.

    PubMed  Google Scholar 

  • Yip, W.K., Moore, T. and Yang, S.F. 1992. Differential accumulation of transcripts for 4 tomato 1-aminocyclopropane-1-carboxylate synthase homologs under various conditions. Proc. Natl. Acad. Sci. USA 89: 2475–2479.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Forest Genetics, Swedish University of Agricultural Sciences, Box 7027, 75007, Uppsala, Sweden

    Anders M Lindroth, Peter Saarikoski, Gunnar Flygh, David Clapham, Roland Grönroos, Roland Grönroos & Sara von Arnold

  2. Department of Molecular, Cell and Developmental Biology, U.C.L.A., P.O. Box 951606, Los Angeles, CA, 90095, USA

    Anders M Lindroth

  3. Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, Box 7026, 75007, Uppsala, Sweden

    Gunnar Flygh

  4. Department of Plant Biology, Swedish University of Agricultural Sciences, Box 7080, SE-75007, Uppsala, Sweden

    Mattias Thelander & Hans Ronne

Authors
  1. Anders M Lindroth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Saarikoski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gunnar Flygh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Clapham
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roland Grönroos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mattias Thelander
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hans Ronne
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sara von Arnold
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lindroth, A.M., Saarikoski, P., Flygh, G. et al. Two S-adenosylmethionine synthetase-encoding genes differentially expressed during adventitious root development in Pinus contorta. Plant Mol Biol 46, 335–346 (2001). https://doi.org/10.1023/A:1010637012528

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010637012528

Search

Navigation