Skip to main content

Advertisement

Log in

Changes in the abundance of sugars and sugar-like compounds in tall fescue (Festuca arundinacea) due to growth in naphthalene-treated sand

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The hydrophilic metabolome of tall fescue (Festuca arundinacea) adapted to grow in naphthalene-treated sand (0.8 g kg−1 sand dw) was analysed using gas chromatography-mass spectrometry, and peaks corresponding to the more abundant compounds were tentatively identified from analysis of their mass spectral features and reference to the NIST Mass Spectral Database. Particular attention was paid to sugars as they are known to play important roles as stress regulators in plants. The results showed that the abundance of sugars was greater in the roots but lesser in the shoots of treated plants when compared to their control counterparts. The results for indole acetic acid (IAA) were notable: IAA was prominently less in the treated roots compared to shoots, and in treated shoots, IAA was particularly subdued compared to untreated shoots consistent with IAA degradation in treated plant tissues. The differences in the molecular phenotype between control and treated plants were expressed in root structural differences. The treated roots were modified to have greater suberisation, enhanced thickening in the endodermis and distortions in the cortical zone as demonstrated through scanning electron and epi-fluorescence microscopy.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Anderson JW, Neff JM, Cox BA, Tatem HE, Hightower GM (1974) Characteristics of dispersions and water soluble extracts of crude and refined oils and their toxicity to estuarine crustaceans and fish. Mar Biol 27:75–88

    Article  CAS  Google Scholar 

  • Balasubramaniyam A, Harvey PJ (2014) Scanning electron microscopic investigations of root structural modifications arising from growth in crude oil-contaminated sand. Environ Sci Pollut R. doi:10.1007/s11356-014-3138-7

    Google Scholar 

  • Bandurski RS, Schulze A, Leznicki A et al (1988) Regulation of the amount of IAA in seedling plants. In: Bandurski RS, Krekule J, Kutacek M (eds) Physiology and biochemistry of auxins in plants. Academia, Praha, pp 21–32

    Google Scholar 

  • Bolouri-Moghaddam MR, Roy KL, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. Review article. FEBS J 277:2022–2037

    Article  CAS  Google Scholar 

  • Brundrett MC, Enstone DE, Peterson CA (1988) A berberine-aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146:133–142

  • Couee I, Sulmon C, Gouesbet G, Amrani EI (2006) An involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459

    Article  CAS  Google Scholar 

  • Du H, Wang Z, Yu W, Liu Y, Huang B (2011) Differential metabolic responses of perennial grass Cynodon transvaalensis × Cynodon dactylon (C4) and Poa Pratensis (C3) to heat stress. Physiol Plantarum 141:251–264

    Article  CAS  Google Scholar 

  • Ehrlich GG, Goerlitz DF, Godsy EM, Hult MF (1982) Degradation of phenolic contaminants in ground water by anaerobic bacteria: St. Louis Park, Minnesota. Ground Water 20:703–710

    Article  CAS  Google Scholar 

  • Farrell-Jones J (2003) Petroleum hydrocarbons and polyaromatic hydrocarbons. In: Thompson CK, Nathanail PC (eds) 2003. Chemical analysis of contaminated land. Blackwell Publishing Ltd

  • Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu Rev Plant Physiol Plant Mol Biol 37:165–186

    Article  CAS  Google Scholar 

  • Gaspar T, Penel C, Hagege D et al (1991) Peroxidases in plant growth, differentiation and development processes. In: Lobarzewski J, Greppin H, Penel C, Gaspar T (eds) Biochemical, molecular and physiological aspects of plant peroxidases. University of Geneva, Switzerland, pp 249–280

    Google Scholar 

  • Grambow HJ (1986) Pathway and mechanism of the peroxidase catalyzed degradation of indole-3-acetic acid. In: Greppin H, Penel C, Gaspar T (eds) Molecular and physiological aspects of plant peroxidases. University of Geneva, Switzerland, pp 31–41

    Google Scholar 

  • Gromova M, Roby C (2010) Toward Arabidopsis thaliana hydrophilic metabolome: assessment of extraction methods and quantitative 1H NMR. Technical focus. Physiol Plantarum 140:111–127

    Article  CAS  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  CAS  Google Scholar 

  • Harms HH (1992) In-vitro systems for studying phytotoxicity and metabolic fate of pesticides and xenobiotics in plants. Pestic Sci 35:277–281

    Article  CAS  Google Scholar 

  • Harvey PJ, Campanella BF, Castro PML, Harms H, Lichtfouse E, Schaffner AR, Smrcek S, Werck-Reichhart D (2002) Phytoremediation of polyaromatic hydrocarbons, anilines and phenols. Review articles: phytoremediation. Environ Sci Pollut R 9:29–47

    Article  CAS  Google Scholar 

  • Heitzer A, Webb OF, Thonnard JE, Sayler GS (1992) Specific and quantitative assessment of naphthalene and salicylate bioavailability by using a bioluminescent catabolic reporter bacterium. Appl Environ Microb 58:1839–1846

    CAS  Google Scholar 

  • Higashiyama T (2002) Novel functions and applications of trehalose. Pure Appl Chem 74:1263–1269

    Article  CAS  Google Scholar 

  • Janska M, Hajslova J, Tomaniova M, Kocourek V, Vavrova M (2006) Polycyclic aromatic hydrocarbons in fruits and vegetables grown in the Czech Republic. Bull Environ Contam Toxicol 77:492–499

    Article  CAS  Google Scholar 

  • Johnson DL, Maguire KL, Anderson DR, McGrath SP (2004) Enhanced dissipation of chrysene in planted soil: the impact of a rhizobial inoculum. Soil Biol Biochem 36:33–38

  • Kim HK, Verpoorte R (2009) Sample preparation for plant metabolomics. Phytochem Anal. doi:10.1002/pca.1188

    Google Scholar 

  • Liste HH, Alexander M (2000) Plant promoted pyrene degradation in soil. Chemosphere 40:7–10

    Article  CAS  Google Scholar 

  • Machackova I, Ullmann J, Krekule J, Opatrny Z (1988) Comparison of in vivo IAA decarboxylation rate with in vitro peroxidase, IAA oxidase activities. In: Bandurski RS, Krekule J, Kutacek R (eds) Physiology and biochemistry of auxins in plants. Academia, Praha, pp 87–91

    Google Scholar 

  • Mattson M, Calabrese E (2008) When a little poison is good for you. NewScientist. http: //www.NewScientist.com. Accessed 06 August 2008

  • Meulenberg R, Rijnaarts HHHM, Doddema HJ, Field JA (1997) Partially oxidised polycyclic aromatic hydrocarbons show an increased bioavailability and biodegradability. FEMS Microbiol Lett 152:45–49

    Article  CAS  Google Scholar 

  • Pego JV, Kortstee AJ, Huijser C, Smeekens SCM (2000) Photosynthesis, sugars and the regulation of gene expression. J Exp Bot 51:407–416

    Article  CAS  Google Scholar 

  • Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signalling. The Arabidopsis book. American Society of Plant Biologists. doi:10.1199/tab.0117

  • Ritsema T, Brodmann D, Diks SH, Bos CL, Nagaraj V, Pieterse CMJ, Boller T, Wiemken A, Peppelenbosch MP (2009) Are small GTPases signal hubs in sugar mediated induction of fructan biosynthesis? PLoS One 4(8), doi:10.1371/journal.pone.0006605

  • Rolland F, Winderickx J, Thevelein JM (2001) Glucose sensing mechanisms in eukaryotic cells. Trends Biochem Sci 26:310–317

    Article  CAS  Google Scholar 

  • Siciliano SD, Germida JJ, Banks K, Greer CW (2003) Changes in microbial composition and function during a polyaromatic hydrocarbon phytoremediation field trial. Appl Environ Microbiol 69:483–489

    Article  CAS  Google Scholar 

  • Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59–63

    Article  CAS  Google Scholar 

  • Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646

    Article  CAS  Google Scholar 

  • Sutherland JB (1992) Detoxification of polycyclic aromatic hydrocarbons by fungi. J Ind Microbiol 9:53–62

    Article  CAS  Google Scholar 

  • Thomas JM, Yordy JR, Amador JA et al (1986) Rates of dissolution and biodegradation of water-insoluble organic compounds. Appl Environ Microb 52:290–296

    CAS  Google Scholar 

  • Troquet J, Larroche C, Dussap CG (2003) Evidence for the occurrence of an oxygen limitation during soil bioremediation by solid-state fermentation. Biochem Eng J 13:103–112

    Article  CAS  Google Scholar 

  • U.S. Department of Health and Human Services (2005) Toxicological profile for naphthalene, 1-methylnaphthalene, and 2-methylnaphthalene. Agency for Toxic Substances and Disease Registry, Georgia. http://www.atsdr.cdc.gov/toxprofiles/tp67.pdf. Accessed 16 April 2012

  • Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60:9–18

    Article  Google Scholar 

  • Vandevivere P, Verstraete W (2001) Environmental applications. In: Ratledge C, Kristiansen B (eds) Basic biotechnology, Secondth edn. Cambridge University Press, London, pp 531–557

    Google Scholar 

  • Weber AP, Schwacke R, Flugge UI (2005) Solute transporters of the plastid envelope membrane. Annu Rev Plant Biol 56:133–164

    Article  Google Scholar 

  • Weissenfels WD, Klewer HJ, Langhoff J (1992) Adsorption of polycyclic aromatic hydrocarbons (PAHs) by soil particles: influence on biodegradability and biotoxicity. Appl Microbiol Biot 36:689–696

    Article  CAS  Google Scholar 

  • Wild E, Dent J, Thomas GO, Jones KC (2005) Direct observation of organic contaminant uptake, storage and metabolism within plant roots. Environ Sci Technol 39:3695–3702

    Article  CAS  Google Scholar 

  • Wilson S, Jones K (1993) Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): a review. Environ Pollut 81:229–249

    Article  CAS  Google Scholar 

  • Zacchi L, Morris I, Harvey PJ (2000) Disordered ultrastructure in lignin-peroxidase-secreting hyphae of the white-rot fungus Phanerochaete chrysosporium. Microbiology 146:759–765

    CAS  Google Scholar 

  • Yamazaki I, Yokota K (1965) Conversion of ferrous peroxidase into compound III in the presence of NADH. Biochem Bioph Res 21:582–586

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Professor Francis S Pullen and Dr. Kai Law for their suggestions on mass spectrometric work and Dr. Mark M Chapman for his suggestions on microscopic study, Professor Anthony I Mallet for his insightful comments on the draft of this manuscript and Dr. Stephen Young for his guidance on statistical interpretation of the data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anuluxshy Balasubramaniyam.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Balasubramaniyam, A., Harvey, P.J. Changes in the abundance of sugars and sugar-like compounds in tall fescue (Festuca arundinacea) due to growth in naphthalene-treated sand. Environ Sci Pollut Res 22, 5817–5830 (2015). https://doi.org/10.1007/s11356-014-3812-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3812-9

Keywords

Navigation