Skip to main content
Log in

Influence of N nutrients on GS activity and putative ammonium transporter1;2 (SaAMT1;2) expression in sandal plants (Santalum album L.)

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Ammonium acts as better N source for sandal growth. The ammonium assimilation and transport is mediated by the up-regulation of putative leaf and root SaAMT1;2 in Santalum album.

Abstract

Nitrogen compounds play a major role in the concentration of macromolecules and expression of putative ammonium transporter1;2 (SaAMT1;2) in Santalum album (S. album) hydroponic cultures. Specific activity of glutamine synthetase (GS) and putative SaAMT1;2 expression levels were determined on the 7th, 14th and 21st day in S. album grown in nitrogen-free Hoagland’s solution supplemented with different concentrations (0-10 mM) of ammonium nitrate (NH4NO3), ammonium sulphate [NH4(SO4)2] and potassium nitrate (KNO3). Highest glutamine synthetase (GS) specific activity was observed in 0.5 mM KNO3 on the 14th day and chlorophyll content in 0.5 mM NH4NO3 on the 7th and 21st day. Highest quantity of total sugar and soluble sugar was detected in 0.5 mM NH4NO3 on the 14th day. The putative leaf and root SaAMT1;2 expression levels were positively correlated to GS specific activity, however, NH4(SO4)2 did not appreciably influence the GS specific activity and putative SaAMT1;2 expressions during the initial days. The relative expression of putative SaAMT1;2 followed an identical pattern in the NH4NO3/NH4(SO4)2 treated plants on the 7th and 21st day. The biochemical and molecular parameters indicated improved NH3 assimilation in hydroponic S. album cultures supplemented with different N compounds; however, it is time and concentration dependent.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Apuzzo E, Rogato A, Simon-Rosin U, Alaoui H, Barbulova A, Betti M, Udvardi MK (2004) Characterization of three functional high-affinity ammonium transporters in Lotus japonicas with differential transcriptional regulation and spatial expression. Plant Physiol 134:1763–1774

    Article  PubMed  PubMed Central  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bojovic B, Markovic A (2009) Correlation between nitrogen and chlorophyll content in wheat (Triticum aestivum L.). Kragujev J Sci 31:69–74

    Google Scholar 

  • Brown H, Watt M, Clinton P, Marson E (2010) Influence of ammonium nitrate supply on growth, dry matter partitioning, N uptake and photosynthetic capacity of Pinus radiata seedlings. Trees 24:1097–1107

    Article  Google Scholar 

  • Camanes G, Cerezo M, Primo-Millo E, Gojon A, García-Agustin P (2009) Ammonium transport and CitAMT1 expression are regulated by N in Citrus plants. Planta 229:331–342

    Article  CAS  PubMed  Google Scholar 

  • Comadira G, Rasool B, Karpinska B, Morris J, Verrall SR, Hedley PE, Hancock RD (2015) Nitrogen deficiency in barley (Hordeum vulgare) seedlings induces molecular and metabolic adjustments that trigger aphid resistance. J Exp Bot 66(12):3639–3655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper HD, Clarkson DT (1989) Cycling of amino nitrogen and other nutrients between shoots and roots in cereals. J Exp Bot 40:753–762

    Article  CAS  Google Scholar 

  • Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crawford NM, Glass AD (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3:389–395

    Article  Google Scholar 

  • Dai G, Deblois CP, Liu S, Juneau P, Qiu B (2008) Differential sensitivity of five cyanobacterial strains to ammonium toxicity and its inhibitory mechanism on the photosynthesis of rice-field cyanobacterium Ge–Xian–Mi (Nostoc). Aquat Toxicol 89:113–121

    Article  CAS  PubMed  Google Scholar 

  • Deepa P, Yusuf A (2015) Histological and biochemical evaluation of Santalum album L. seedlings cocultivated with different hosts. Ann Plant Sci 4:1016–1021

    Google Scholar 

  • Deepa P, Yusuf A (2016) Influence of different host associations on glutamine synthetase activity and ammonium transporter in Santalum album L. Physiol Mol Biol Plants 22(3):331–340. doi:10.1007/s12298-016-0368-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deepa K, Sheeja TE, Santhi R, Sasikumar B, Cyriac A, Deepesh PV, Prasath D (2014) A simple and efficient protocol for isolation of high quality functional RNA from different tissues of turmeric (Curcuma longa L.). Physiol Mol Biol Plants 20:263–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Druege U, Zerche S, Kadner R, Ernst M (2000) Relation between nitrogen status, carbohydrate distribution and subsequent rooting of chrysanthemum cuttings as affected by pre-harvest nitrogen supply and cold-storage. Ann Bot 85:687–701

    Article  CAS  Google Scholar 

  • Glass AD, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864

    Article  CAS  PubMed  Google Scholar 

  • Hamayun M, Gul H, Khan SA, Ullah Z (2014) Effect of potassium nitrate and salinity on growth and endogenous gibberellins of Glycine max Var. Daewonkong. Pakhtunkhwa J Life Sci 02(03/04):96–105

    Google Scholar 

  • Hedge JE, Hofreiter BT (1962) In: Whistler RL, Be Miller JN (eds) Cabohydrate chemistry, vol 17. Academic Press, New York, p 420

  • Ishiyama K, Inoue E, Watanabe-Takahashi A, Obara M, Yamaya T, Takahashi H (2004) Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis. J Biol Chem 279:16598–16605

    Article  CAS  PubMed  Google Scholar 

  • Kan CC, Chung TY, Hsieh MH (2015) Gene expression profiling of rice seedlings in response to glutamine treatment. Genom Data 6:123–124

    Article  PubMed  PubMed Central  Google Scholar 

  • Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53:773–787

    Article  CAS  PubMed  Google Scholar 

  • Linka N, Weber APM (2010) Intracellular metabolite transporters in plants. Mol Plant 3(1):21–53

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{{ - \Delta \Delta C_{\text{T}} }}\) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Ludewig U, Neuhauser B, Dynowski M (2007) Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Lett 581:2301–2308

    Article  CAS  PubMed  Google Scholar 

  • Masclaux-Daubresse C, Daniel Verdile F, Dechorghat J, Charden F, Ganfichan L, Suzuki A (2010) Nitrogen uptake and assimilation in plants: challenges for sustainable and productive agriculture. Ann Bot 105:1141–1157

    Article  PubMed  PubMed Central  Google Scholar 

  • Metcalfe RJ, Nault J, Hawkins BJ (2011) Adaptation to nitrogen form: comparing inorganic N and aminoacid availability and uptake of four temperate forest plants. Can J For Res 41:1626–1637

    Article  CAS  Google Scholar 

  • Misra BB, Dey S (2013) Developmental variations in sesquiterpenoid biosynthesis in East Indian sandalwood tree (Santalum album L.). Trees 27(4):1071–1086

    Article  CAS  Google Scholar 

  • Munzi S, Pisani T, Paoli L, Renzi M, Loppi S (2013) Effect of nitrogen supply on the C/N balance in the lichen Evernia prunastri (L.) Ach. Turk J Biol 37:165–170

    CAS  Google Scholar 

  • Nagaveni HC, Vijayalakshmi G (2003) Growth performance of sandal (Santalum album L.) with different host species. Sandalwood Res Newsl 18:1–4

    Google Scholar 

  • Nicodemus MA, Salifu FK, Jacobs DF (2008) Growth, nutrition, and photosynthetic response of black walnut to varying nitrogen sources and rates. J Plant Nutr 31:1917–1936

    Article  CAS  Google Scholar 

  • Oliveira IC, Coruzzi GM (1999) Carbon and amino acids reciprocally modulate the expression of glutamine synthetase in Arabidopsis. Plant Physiol 121:301–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omari REI, Reuda-Lopez M, Avila C, Crespillo R, Nhiri M, Canovas FM (2010) Ammonium tolerance and the regulation of two cytosolic glutamine synthetases in the roots of sorghum. Funct Plant Biol 37:55–63. doi:10.1071/FP09162

    Article  Google Scholar 

  • Prinsi B, Espen L (2015) Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize. BMC Plant Biol 15(1):1

    Article  CAS  Google Scholar 

  • Radomiljac AM, McComb JA, Pate JS, Tennakoon KU (1998) Xylem transfer of organic solutes in Santalum album L. (Indian sandalwood) in association with legume and non-legume hosts. Ann Bot 82:675–682

    Article  CAS  Google Scholar 

  • Rao DB, Krishna GM, Rao KVR, Kiran CR, Rao TR (2014) Screening of in vitro cytotoxicity, evaluation of hepato-protective and oxidative stress inhibiting potential Clitoria ternatea in carbon tetrachloride induced hepatic damage in rats. Pharm Commun 4(3):49

    Google Scholar 

  • Rocha D, Ashokan PK, Santhoshkumar AV, Anoop EV, Sureshkumar P (2014) Influence of host plant on the physiological attributes of field-grown sandal tree (Santalum album). J Trop For Sci 166–172

  • Sahrawy M, Avila C, Chueca A, Canovas FM, Lopez-Gorge J (2004) Increased sucrose level and altered nitrogen metabolism in Arabidopsis thaliana transgenic plants expressing antisense chloroplastic fructose-1, 6-bisphosphatase. J Expl Bot 55(408):2495–2503

    Article  CAS  Google Scholar 

  • Sanchez-Zabala J, Gonzalez-Murua C, Marino D (2015) Mild ammonium stress increases chlorophyll content in Arabidopsis thaliana. Plant Signal Behav 10(3):e991596

    Article  PubMed  PubMed Central  Google Scholar 

  • Serapiglia MJ, Minocha R, Minoch SC (2008) Changes in polyamines, inorganic ions and glutamine synthetase activity in response to nitrogen availability and form in red spruce (Picea rubens). Tree Physiol 28(12):1793–1803

    Article  CAS  PubMed  Google Scholar 

  • Shapiro BM, Stadtman ER (1970) Glutamine synthetase (Escherichia coli). M Enzymol 17:910–922

    Article  Google Scholar 

  • Simonovic AD, Anderson MD (2008) Light modulates activity and expression of glutamine synthetase isoforms in maize seedling roots. Arch Biol Sci 60:649–660

    Article  Google Scholar 

  • Sonoda Y, Ikeda A, Saiki S, von Wiren N, Yamaya T, Yamaguchi J (2003) Distinct expression and function of three ammonium transporter genes (OsAMT1;1-1;3) in rice. Plant Cell Physiol 44:726–734

    Article  CAS  PubMed  Google Scholar 

  • Straub D, Ludewig U, Neuhauser B (2014) A nitrogen-dependent switch in the high affinity ammonium transport in Medicago truncatula. Plant Mol Biol 86:485–494

    Article  CAS  PubMed  Google Scholar 

  • Suarez MF, Avila C, Gallardo F, Canton FR, Gutierrez AG, Claros MG, Canovas FM (2002) Molecular and enzymatic analysis of ammonium assimilation in woody plants. J Exp Bot 53:891–904

    Article  CAS  PubMed  Google Scholar 

  • Suenaga A, Moriya K, Sonoda Y, Ikeda A, von Wiren N, Hayakawa T, Yamaya T (2003) Constitutive expression of a novel-type ammonium transporter OsAMT2 in rice plants. Plant Cell Physiol 44:206–211

    Article  CAS  PubMed  Google Scholar 

  • Temple SJ, Kunjibettu S, Roche D, Sengupta-Gopalan C (1996) Total glutamine synthetase activity during soybean nodule development is controlled at the level of transcription and holoprotein turnover. Plant Physiol 112(4):1723–1733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tischner R (2000) Nitrate uptake and reduction in higher and lower plants. Plant Cell Environ 23(10):1005–1024

    Article  CAS  Google Scholar 

  • Trueman LJ, Richardson A, Forde BG (1996) Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans. Gene 175(1):223–231

    Article  CAS  PubMed  Google Scholar 

  • von Wiren N, Lauter FR, Ninnemann O, Gillissen B, Walch-Liu P, Engels C, Jost W, Frommer WB (2000) Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. Plant J 21:167–175

    Article  Google Scholar 

  • Zheng ZL (2009) Carbon and nitrogen nutrient balance signaling in plants. Plant Signal Behav 4:584–591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Director, Interuniversity Centre for Plant Biotechnology, Department of Botany, University of Calicut, Kerala for providing the facilities. D. P. acknowledges University of Calicut for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Yusuf.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by H. Rennenberg.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yusuf, A., Deepa, P. Influence of N nutrients on GS activity and putative ammonium transporter1;2 (SaAMT1;2) expression in sandal plants (Santalum album L.). Trees 31, 1773–1784 (2017). https://doi.org/10.1007/s00468-017-1583-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-017-1583-x

Keywords

Navigation