Skip to main content
SpringerLink
Log in

Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

The polyamine metabolic pathway is intricately connected to metabolism of several amino acids. While ornithine and arginine are direct precursors of putrescine, they themselves are synthesized from glutamate in multiple steps involving several enzymes. Additionally, glutamate is an amino group donor for several other amino acids and acts as a substrate for biosynthesis of proline and γ-aminobutyric acid, metabolites that play important roles in plant development and stress response. Suspension cultures of poplar (Populus nigra × maximowiczii), transformed with a constitutively expressing mouse ornithine decarboxylase gene, were used to study the effect of up-regulation of putrescine biosynthesis (and concomitantly its enhanced catabolism) on cellular contents of various protein and non-protein amino acids. It was observed that up-regulation of putrescine metabolism affected the steady state concentrations of most amino acids in the cells. While there was a decrease in the cellular contents of glutamine, glutamate, ornithine, arginine, histidine, serine, glycine, cysteine, phenylalanine, tryptophan, aspartate, lysine, leucine and methionine, an increase was seen in the contents of alanine, threonine, valine, isoleucine and γ-aminobutyric acid. An overall increase in percent cellular nitrogen and carbon content was also observed in high putrescine metabolizing cells compared to control cells. It is concluded that genetic manipulation of putrescine biosynthesis affecting ornithine consumption caused a major change in the entire ornithine biosynthetic pathway and had pleiotropic effects on other amino acids and total cellular carbon and nitrogen, as well. We suggest that ornithine plays a key role in regulating this pathway.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Azevedo R, Lancien M, Lea P (2006) The aspartic acid metabolic pathway, an exciting and essential pathway in plants. Amino Acids 30:143–162

    Article  CAS  PubMed  Google Scholar 

  • Aziz A, Larher F (1995) Changes in polyamine titers associated with the proline response and osmotic adjustment of rape leaf discs submitted to osmotic stress. Plant Sci 112:175–186

    Article  CAS  Google Scholar 

  • Aziz A, Martin-Tanguy J, Larher F (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol Plant 104:195–202

    Article  CAS  Google Scholar 

  • Bhatnagar P, Glasheen B, Bains S, Long S, Minocha R, Walter C, Minocha S (2001) Transgenic manipulation of the metabolism of polyamines in poplar cells. Plant Physiol 125:2139–2153

    Article  CAS  PubMed  Google Scholar 

  • Bhatnagar P, Minocha R, Minocha S (2002) Genetic manipulation of the metabolism of polyamines in poplar cells: the regulation of putrescine catabolism. Plant Physiol 128:1455–1469

    Article  CAS  PubMed  Google Scholar 

  • Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115

    Article  PubMed  Google Scholar 

  • Bourguignon J, Rébeillé F, Douce R (1999) Serine and glycine metabolism in higher plants. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. CRC, Boca Raton, pp 111–146

    Google Scholar 

  • Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909–9914

    Article  CAS  PubMed  Google Scholar 

  • Coruzzi G, Last R (2000) Amino acids. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 358–410

    Google Scholar 

  • Curien GL M, Robert-Genthon M, Dumas R (2007) Allosteric monofunctional aspartate kinases from Arabidopsis. FEBS J 274:64–176

    Google Scholar 

  • de Sousa CAF, Sodek L (2003) Alanine metabolism and alanine aminotransferase activity in soybean (Glycine max) during hypoxia of the root system and subsequent return to normoxia. Environ Exp Bot 50:1–8

    Article  Google Scholar 

  • Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13:14–19

    Article  CAS  PubMed  Google Scholar 

  • Ferrario-Méryl S, Suzuki A, Kunz C, Valadier M, Roux Y, Hirel B, Foyer C (2000) Modulation of amino acid metabolism in transformed tobacco plants deficient in FD-GOGAT. Plant Soil 221:67–79

    Article  Google Scholar 

  • Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358

    Article  CAS  PubMed  Google Scholar 

  • Foyer C, Parry M, Noctor G (2003) Markers and signals associated with nitrogen assimilation in higher plants. J Exp Bot 54:585–593

    Article  CAS  PubMed  Google Scholar 

  • Gallardo F, Fu J, Jing Z, Kirby E, Cánovas F (2003) Genetic modification of amino acid metabolism in woody plants. Plant Physiol Biochem 41:587–594

    Article  CAS  Google Scholar 

  • Halgand F, Wessel P, Laprevote O, Dumas R (2002) Biochemical and mass spectrometric evidence for quaternary structure modifications of plant threonine deaminase induced by isoleucine. Biochemistry 41:13767–13773

    Article  CAS  PubMed  Google Scholar 

  • Hoefgen R, Hesse H (2007) Sulfur in plants as part of a metabolic network. In: Hawkesford MJ, De Kok LJ (eds) Sulfur in plants: an ecological perspective. Springer, Berlin, pp 107–142

    Chapter  Google Scholar 

  • Houdusse F, Zamarreño A, Garnica M, García-Mina J (2005) The importance of nitrate in ameliorating the effects of ammonium and urea nutrition on plant development: the relationships with free polyamines and plant proline contents. Funct Plant Biol 32:1057–1067

    Article  CAS  Google Scholar 

  • Kocsy G, Laurie R, Szalai G, Szilagyi V, Simon-Sarkadi L, Galiba G, Ja De Ronde JA (2005) Genetic manipulation of proline levels affects antioxidants in soybean subjected to simultaneous drought and heat stresses. Physiol Plant 124:227–235

    Article  CAS  Google Scholar 

  • Kumar A, Minocha S (1998) Transgenic manipulation of polyamine metabolism. In: Lindsey K (ed) Transgenic plant research. Harwood, Amsterdam, pp 187–199

    Google Scholar 

  • Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research in 2007. J Plant Res 120:345–350

    Article  CAS  PubMed  Google Scholar 

  • Liu J-H, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126

    CAS  Google Scholar 

  • Mattoo AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear Magnetic Resonance spectroscopy based metabolite profiles of transgenic tomato fruit engineered to accumulate polyamines spermidine and spermine reveal enhanced anabolic nitrogen-carbon interactions. Plant Physiol 142:1759–1770

    Article  CAS  PubMed  Google Scholar 

  • Mazzucotelli E, Tartari A, Cattivelli L, Forlani G (2006) Metabolism of γ-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot 57:3755–3766

    Article  CAS  PubMed  Google Scholar 

  • Miflin B, Habash D (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 53:979–987

    Article  CAS  PubMed  Google Scholar 

  • Miller AJ, Fan X, Shen Q, Smith SJ (2007) Amino acids and nitrate as signals for the regulation of nitrogen acquisition. J Exp Bot 59:111–119

    Article  PubMed  Google Scholar 

  • Minocha R, Shortle WC, Long SL, Minocha SC (1994) A rapid and reliable procedure for extraction of cellular polyamines and inorganic ions from plant tissues. J Plant Growth Regul 13:187–193

    Article  CAS  Google Scholar 

  • Mohapatra S, Minocha R, Long S, Minocha S (2009) Putrescine overproduction negatively impacts the oxidative state of poplar cells in culture. Plant Physiol Biochem 47:262–271

    Article  CAS  PubMed  Google Scholar 

  • Morandini P (2009) Rethinking metabolic control. Plant Sci 176:441–451

    Article  CAS  Google Scholar 

  • Morris S (2007) Arginine metabolism: boundaries of our knowledge. J Nutr 137:1602S–1609S

    CAS  PubMed  Google Scholar 

  • Page A, Mohapatra S, Minocha R, Minocha SC (2007) The effects of genetic manipulation of putrescine biosynthesis on transcription and activities of the polyamine biosynthetic enzymes. Physiol Plant 129:707–724

    Article  CAS  Google Scholar 

  • Quan Y, Minocha R, Minocha SC (2002) Genetic manipulation of polyamine metabolism in poplar II: effects on ethylene biosynthesis. Plant Physiol Biochem 40:929–937

    Article  CAS  Google Scholar 

  • Raman S, Rathinasabapathi B (2004) Pantothenate synthesis in plants. Plant Sci 167:961–968

    Article  CAS  Google Scholar 

  • Rhodes D, Verslues PE, Sharp RE (1999) Role of amino acids in abiotic stress resistance. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. CRC, Boca Raton, pp 319–356

    Google Scholar 

  • Roosens N, Bitar F, Loenders K, Angenon G, Jacobs M (2002) Overexpression of ornithine- δ-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Mol Breed 9:73–80

    Article  CAS  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

    Article  CAS  PubMed  Google Scholar 

  • Sharma S, Dietz K (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726

    Article  CAS  PubMed  Google Scholar 

  • Siehl DL (1999) The biosynthesis of tryptophan, tyrosine, and phenylalanine from chorismate. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. CRC, Boca Raton, pp 171–204

    Google Scholar 

  • Simon-Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, De Ronde J (2005) Genetic manipulation of proline accumulation influences the concentrations of other amino acids in soybean subjected to simultaneous drought and heat stress. J Agric Food Chem 53:7512–7517

    Article  CAS  PubMed  Google Scholar 

  • Simon-Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, De Ronde JA (2006) Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Plant Biol 50:793–796

    Article  CAS  Google Scholar 

  • Singh B (1999a) Plant amino acids: Biochemistry and biotechnology. CRC, Boca Raton

    Google Scholar 

  • Singh B (1999b) Biosynthesis of valine, leucine and isoleucine. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. CRC, Boca Raton, pp 227–247

    Google Scholar 

  • Slocum R (2005) Genes, enzymes and regulation of arginine biosynthesis in plants. Plant Physiol Biochem 43:729–745

    Article  CAS  PubMed  Google Scholar 

  • Székely G, Ábrahám E, Cséplö A, Rigó G, Zsgimond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28

    Article  PubMed  Google Scholar 

  • Terano S, Suzuki Y (1978) Formation of β-alanine from spermine and spermidine in maize shoots. Phytochemistry 17:148–149

    Article  CAS  Google Scholar 

  • Weber A, Flügge U (2002) Interaction of cytosolic and plastidic nitrogen metabolism in plants. J Exp Bot 53:865–874

    Article  CAS  PubMed  Google Scholar 

  • Zhu X, Galili G (2003) Increased lysine synthesis coupled with a knockout of its catabolism synergistically boosts lysine content and also transregulates the metabolism of other amino acids in Arabidopsis seeds. Plant Cell 15:845–853

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was partially supported by the USDA-NRI award No. 2002-35318-12674, the NH Agricultural Experiment Station, and the US Forest Service, Northern Research Station. The authors would like to thank Jane Hislop, US Forest Service for help in analysis of total C and total N.

Author information

Author notes

  1. Sridev Mohapatra

    Present address: Department of Biology, University of Texas, Arlington, TX, 76019, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of New Hampshire, Durham, NH, 03824, USA

    Sridev Mohapatra & Subhash C. Minocha

  2. Northern Research Station, USDA Forest Service, 271 Mast Road, Durham, NH, 03824, USA

    Rakesh Minocha & Stephanie Long

Authors
  1. Sridev Mohapatra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rakesh Minocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephanie Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Subhash C. Minocha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Subhash C. Minocha.

Additional information

Scientific Contribution No. 2384 from the New Hampshire Agricultural Experiment Station.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 46 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mohapatra, S., Minocha, R., Long, S. et al. Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids. Amino Acids 38, 1117–1129 (2010). https://doi.org/10.1007/s00726-009-0322-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-009-0322-z

Keywords

Search

Navigation