Skip to main content
SpringerLink
Log in

High Molecular Size Humic Substances Enhance Phenylpropanoid Metabolism in Maize (Zea mays L.)

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

A high molecular weight humic fraction (>3,500 Da) was characterized chemically by DRIFT and 1H NMR spectroscopy, and was applied to Zea mays L. plants to evaluate its effect on phenylpropanoid metabolism. The activity and gene expression of phenylalanine (tyrosine) ammonia-lyase (PAL/TAL), and the concentrations of phenolics and their amino acid precursors phenylalanine and tyrosine were assayed. Maximum induction of PAL/TAL activity and expression was obtained when the concentration of added humic substance was 1 mg C/l hydroponic solution. Phenylalanine and tyrosine significantly decreased (−16% and −22%, respectively), and phenolic compounds increased in treated plants. The effects of the humic substance could be ascribed partly to indoleacetic acid (27 nmol/mg C) in the humic fraction. Our results suggest that this humic fraction induces changes in phenylpropanoid metabolism. This is the first study that shows a relationship between humic substances and the phenylpropanoid 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

Similar content being viewed by others

References

  • Andersen, J. R., Zein, I., Wenzel, G., Krützfeldt, B., Eder, J., Ouzunova, M., and Lübberstedt, T. 2007. High levels of linkage disequilibrium and associations with forage quality at a phenylalanine ammonia-lyase locus in European maize (Zea mays L.) inbreds. Theor. Appl. Genet. 114:307–319.

    Article  CAS  PubMed  Google Scholar 

  • Arnaldos, T. L., Muñoz, R., Ferrer, M. A., and Calderón, A. A. 2001. Changes in phenol content during strawberry (Fragaria ananassa, cv. Chandler) callus culture. Physiol. Plantarum 113:315–322.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Buer, C. S., and Muday, G. K. 2004. The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. The Plant Cell. 16:1191–1205.

    Article  CAS  PubMed  Google Scholar 

  • Canellas, L. P., Olivares, F. L., Okorokova-Façanha, A. L., and Façanha, A. R. 2002. Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H + -ATPase activity in maize roots. Plant Physiol. 130:1951–1957.

    Article  CAS  PubMed  Google Scholar 

  • Canellas, L. P., Teixeira Junior, L. R. L., Dobbss, L. B., Silva, C. A., Medici, L. O., Zandonadi, D. B., and Façanha, A. R. 2008. Humic acids crossinteractions with root and organic acids. Ann. Appl. Biol. 153:157–166.

    CAS  Google Scholar 

  • Canellas, L. P., Piccolo, A., Dobbss, L. B., Spaccini, R., Olivares, F. L., Zandonadi, D. B., and Façanha, A. R. 2010. Chemical composition and bioactivity properties of size-fractions separated from a vermicompost humic acid. Chemosphere 78:457–466.

    Article  CAS  PubMed  Google Scholar 

  • Cánovas, F. M., Cantón, F. R., Gallardo, F., Garcia-Gutierrez, A., and De Vicente, A. 1991. Accumulation of glutamine synthetase during early development of maritime pine (Pinus pinaster) seedlings. Planta 185:372–378.

    Article  Google Scholar 

  • Cavani, L., Ter Halle, A., Richard, C., and Ciavatta, C. 2006. Photo-sensitizing properties of protein hydrolysates-based fertilizers. J. Agric. Food Chem. 54:9160–9167.

    Article  CAS  PubMed  Google Scholar 

  • Dixon, R. A., and Paiva, N. L. 1995. Stress-induced phenylpropanoid metabolism. The Plant Cell 7:1085–1097.

    Article  CAS  PubMed  Google Scholar 

  • Eyheraguibel, B., Silvestre, J., and Morard, P. 2008. Effects of humic substances derived from organic waste enhancement on the growth and mineral nutrition of maize. Bioresour. Technol. 99:4206–4212.

    Article  CAS  PubMed  Google Scholar 

  • Fan, T. W. M. 1996. Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog. Nucl. Mag. Res. Sp. 28:161–219.

    CAS  Google Scholar 

  • Fao–Issds, 1999. World Reference Base for Soil Resources. Istituto Sperimentale per lo Studio e la Difesa del Suolo, Firenze, Italy.

  • Hoagland, D. R., and Arnon, D. 1950. The water culture method for growing plants without soil. Agricultural Experimental Station Circular 347. University of California, CA.

  • Kaufmann iii, G. L., Kneivel, D., and Watschke, T. L. 2007. Effects of a biostimulant on the heat tolerance associated with photosynthetic capacity, membrane thermostability, and polyphenol production of perennial ryegrass. Crop Sci. 47:261–267.

  • Kim, H. J., Fonseca, J. M., Choi, J. H., and Kubota, C. 2007. Effect of methyl jasmonate on phenolic compounds and carotenoids of romaine lettuce (Lactuca sativa L.). J. Agric. Food Chem. 55:10366–10372.

    Article  CAS  PubMed  Google Scholar 

  • Le Floch, G., Rey, P., Benizri, E., Benhamou, N., and Tirilly, Y. 2003. Impact of auxin-compounds produced by the antagonistic fungus Pythium oligandrum or the minor pathogen Pythium group F on plant growth. Plant Soil 257:459–470.

  • Lewis, D., Muday, R., and Gloria, K. 2008. The phenylpropanoid pathway is differentially induced by auxin and ethylene, pp. 125, in J. Friesner, X. Chen, J. Kieber, C. Chang, G. Haughn, S. Poethig, J. Schroeder, T. Western, and H. Zheng (eds.). Proceedings of the 19th International Conference on Arabidopsis Research. The North American Arabidopsis Steering Committee, Montreal, Canada.

  • Maggioni, A., and Renosto, F. 1980. Profilo amminoacidico e valore nutritivo della proteina di Agaricus bisporus (Lange) Fing. e di Agaricus botorquis (Quélet) Saccardo. Agricoltura Italiana 109:237–246.

    Google Scholar 

  • Meenakshi, S., Manicka Gnanambigai, D., Tamil Mozhi, S., Arumugam, M., and Balasubramanian, T. 2009. Total flavanoid and in vitro antioxidant activity of two seaweeds of Rameshwaram Coast. Glob. J. Pharmacol. 3:59–62.

  • Mori, T., Sakurai, M., and Sakuta, M. 2001. Effects of conditioned medium on activities of PAL, CHS, DAHP synthase (DS-Co and DS-Mn) and anthocyanin production in suspension cultures of Fragaria ananassa. Plant Sci. 160:355–360.

    Article  CAS  PubMed  Google Scholar 

  • Muscolo, A., Sidari, M., Attinà, E., Francioso, O., Tugnoli, V., and Nardi, S. 2007. Biological activity of humic substances is related to their chemical structure. Soil Sci. Soc. Am. J. 71:75–85.

    Article  CAS  Google Scholar 

  • Nardi, S., Tosoni, M., Pizzeghello, D., Provenzano, M. R., Cilenti, A., Sturaro, A., Rella, R., and Vianello, A. 2005. Chemical characteristics and biological activity of organic substances extracted from soils by root exudates. Soil Sci. Soc. Am. J. 69:2012–2019.

    Article  CAS  Google Scholar 

  • Nardi, S., Muscolo, A., Vaccaro, S., Baiano, S., Spaccini, R., and Piccolo, A. 2007. Relationship between molecular characteristics of soil humic fractions and glycolytic pathway and Krebs cycle in maize seedlings. Soil Biol. Biochem. 39:3138–3146.

    Article  CAS  Google Scholar 

  • Nardi, S., Carletti, P., Pizzeghello, D., and Muscolo, A. 2009. Biological activities of humic substances, pp. 305–339, in N. Senesi, B. Xing, and P. M. Huang (eds.). Volume 2-Biophysico-Chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems. PART I. Fundamentals and impact of mineral-organic-biota interactions on the formation, transformation, turnover, and storage of natural nonliving organic matter (NOM). John Wiley & Sons, Hoboken, New Jersey.

  • Niemeyer, J., Chen, Y., and Bollag, J. M. 1992. Characterization of humic acids, composts, and peat by diffuse reflectance Fourier-transform infrared spectroscopy. Soil Sci. Soc. Am. J. 56:135–140.

    CAS  Google Scholar 

  • Peer, W. A., and Murphy, A. S. 2007. Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci. 12:556–563.

    Article  CAS  PubMed  Google Scholar 

  • Piccolo, A. 2002. The supramolecular structure of humic substances: A novel understanding of humus chemistry and implications in soil science. Adv. Agron. 75:57–134.

    Article  CAS  Google Scholar 

  • Quaggiotti, S., Ruperti, B., Pizzeghello, D., Francioso, O., Tugnoli, V., and Nardi, S. 2004. Effect of low molecular size humic substances on nitrate uptake and expression of genes involved in nitrate transport in maize (Zea mays L.). J. Exp. Bot. 55:803–13.

    Article  CAS  PubMed  Google Scholar 

  • Rösler, J., Krekel, F., Amrhein, N., and Schmid, J. 1997. Maize phenylalanine ammonia-lyase has tyrosine ammonia-lyase activity. Plant Physiol. 113:175–9.

    Article  PubMed  Google Scholar 

  • Russell, L., Stokes, A. R., Macdonald, H., Muscolo, A., and Nardi, S. 2006. Stomatal responses to humic substances and auxin are sensitive to inhibitors of phospholipase A2. Plant Soil 283:175–185.

    Article  CAS  Google Scholar 

  • Schiavon, M., Ertani, A., and Nardi, S. 2008. Effects of an alfalfa protein hydrolysate on the gene expression and activity of enzymes of the tricarboxylic acid (TCA) cycle and nitrogen metabolism in Zea mays L. J. Agric. Food Chem. 6:11800–11808.

    Article  CAS  Google Scholar 

  • Shinya, T., Gális, I., Narisawa, T., Sasaki, M., Fukuda, H., Matsuoka, H., Saito, M., and Matsuoka, K. 2007. Comprehensive analysis of glucan elicitor-regulated gene expression in tobacco BY-2 cells reveals a novel MYB transcription factor involved in the regulation of phenylpropanoid metabolism. Plant Cell Physiol. 48:1404–1413.

    Article  CAS  PubMed  Google Scholar 

  • Schweizer, P., and Erismann, K. H. 1985. Effect of nitrate and ammonium nutrition of nonnodulated Phaseolus vulgaris L. on phosphoenolpyruvate carboxylase and pyruvate kinase activity. Plant Physiol. 78:455–458.

    Article  CAS  PubMed  Google Scholar 

  • Sokal, R. R., and Rohlf, F. J. 1969. Biometry. 1st ed. W.H. Freeman, San Francisco.

  • Stevenson, F. J. 1994. Humus Chemistry: Genesis, Composition, Reactions. John Wiley and Sons, New York.

    Google Scholar 

  • Trevisan, S., Pizzeghello, D., Reperti, B., Francioso, O., Sassi, A., Palme, K., Quaggiotti, S., and Nardi, S. 2009. Humic substances induce lateral root formation and expression of the early auxin-responsive IAA19 gene and DR5 synthetic element in Arabidopsis. Plant Biology in press, 2010.

  • Visser, S. A. 1983. Applications of Van krevelen’s graphical-statistical method for the study of aquatic humic material. Environ. Sci. Technol. 17:412–417.

    Article  CAS  Google Scholar 

  • Zancani, M., Petrussa, E., Krajñáková, J., Casolo, V., Spaccini, R., Piccolo, A., Macrì, F., and Vianello, A. 2009. Effect of humic acids on phosphate level and energetic metabolism of tobacco BY-2 suspension cell cultures. Environ. Exp. Bot. 65:287–295.

    Article  CAS  Google Scholar 

  • Zandonadi, D. B., Canellas, L. P., and Façanha, A. R. 2007. Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H + pumps activation. Planta 225:1583–1595.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was partially supported by a grant from the University of Padova (ex 60%, 2008) awarded to Prof. Serenella Nardi. We are grateful to Dr. Andrea Ertani and Dr. Sara Trevisan for their helpful assistance. The authors would like to thank Professor Ann E. Hagerman for her precious help in the improvement of the manuscript.

Author information

Authors and Affiliations

  1. Department of Agricultural Biotechnologies, University of Padova, Agripolis, Viale dell’Università 16, 35020, Legnaro, Padova, Italy

    Michela Schiavon, Diego Pizzeghello, Silvia Vaccaro & Serenella Nardi

  2. Department of Agriculture and Forest Systems Management, Mediterranean University of Reggio Calabria, 89100, Reggio di Calabria, Italy

    Adele Muscolo

  3. Department of Agroenvironmental Science and Technology, University of Bologna, Viale Fanin 44, 40127, Bologna, Italy

    Ornella Francioso

Authors
  1. Michela Schiavon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diego Pizzeghello
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adele Muscolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Silvia Vaccaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ornella Francioso
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Serenella Nardi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diego Pizzeghello.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schiavon, M., Pizzeghello, D., Muscolo, A. et al. High Molecular Size Humic Substances Enhance Phenylpropanoid Metabolism in Maize (Zea mays L.). J Chem Ecol 36, 662–669 (2010). https://doi.org/10.1007/s10886-010-9790-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-010-9790-6

Key Words

Search

Navigation