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Inhibitory effects of Plantago lanceolata L. on soil N mineralization

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Abstract

Background and aims

Nitrate leaching from intensively cropped soils represents a huge environmental problem. In order to diversify the range of nitrogen management strategies, this investigation is focused on the effects of ribwort plantain, Plantago lanceolata L., and its allelochemicals on soil N mineralization.

Methods

High-performance liquid chromatography was used in this study for phytochemical analysis of the major allelochemicals aucubin, catalpol, and verbascoside. Soil incubation experiments demonstrated a significant suppression of soil N mineralization caused by the incorporation of the iridoid glycoside (IG) aucubin, leaf material of two varieties (P. lanceolata cv. Libor and cv. Arterner), and an aqueous extract of P. lanceolata leaves.

Results

Throughout the growing season, the two varieties conspicuously differed in aucubin and verbascoside contents as well as in leaf dry weight. In soil incubation experiments, incorporated leaf material of both varieties affected long-term low soil nitrate concentrations. Experimental aucubin application resulted in an inhibitory effect on soil N mineralization. This was not true for the IG catalpol. Furthermore, we observed a negative relationship between IG concentrations and inorganic soil nitrogen concentrations when the soil was incubated with aqueous P. lanceolata leaf extract of different concentrations.

Conclusion

This study enforced the hypothesis that allelochemicals of P. lanceolata have an active role in a suppression effect on soil N mineralization. Further research may be necessary to investigate the specific effects of P. lanceolata allelochemicals on the nitrogen cycle.

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Abbreviations

AMO:

Ammonia monooxygenase

BNI:

Biological nitrification inhibition

DM:

Dry mass

DW:

Dry weight

FW:

Fresh weight

Glu:

Glycosyl

HPLC:

High-performance liquid chromatography

IC:

Initial concentration

IG:

Iridoid glycoside

NIS:

Nitrification-inhibiting substances

PBG:

Phenyl-β-d-glucose

RPE:

Ribwort plantain extract

WHC:

Water-holding capacity

References

  • Adair KL, Schwartz E (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of Northern Arizona, USA. Microb Ecol 56:420–426

    Article  PubMed  CAS  Google Scholar 

  • Al-Mamun M, Abe D, Kofujita H, Tamura Y, Sano H (2008) Comparison of the bioactive components of the ecotypes and cultivars of plantain (Plantago lanceolata L.) herbs. Anim Sci J 79:83–88

    Article  CAS  Google Scholar 

  • Alsaadawi IS (1988) Biological suppression of nitrification by selected cultivars of Helianthus annuus L. J Chem Ecol 14:733–741

    Article  Google Scholar 

  • Alsaadawi IS, Al-Uquili JK, Alrubeaa AJ, Al-Hadithy SM (1986) Allelopathic suppression of weed and nitrification by selected cultivars of Sorghum bicolor (L.) Moench. J Chem Ecol 12:209–219

    Article  Google Scholar 

  • Arp DJ, Stein LY (2003) Metabolism of inorganic N compounds by ammonia-oxidizing bacteria. Crit Rev Biochem Mol 38:471–495

    Article  CAS  Google Scholar 

  • Azam F, Haider K, Malik KA (1985) Transformation of 14C labelled plant components in soil in relation to immobilization and remineralization of 15N fertilizer. Plant Soil 86:15–25

    Article  CAS  Google Scholar 

  • Azam F, Mahmood T, Malik KA (1988) Immobilization–remineralization of NO3–N and total N balance during the decomposition of glucose, sucrose and cellulose in soil incubated at different moisture regimes. Plant Soil 107:159–163

    Article  CAS  Google Scholar 

  • Bartholomaeus A, Ahokas J (1995) Inhibition of P-450 by aucubin: is the biological activity of aucubin due to its glutaraldehyde-like aglycone. Toxycol Lett 80:75–83

    Article  CAS  Google Scholar 

  • Biere A, Marak HB, van Damme JMM (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs. Oecologia 140:430–441

    Article  PubMed  Google Scholar 

  • Blacquière T (1986) Nitrate reduction in the leaves and numbers of nitrifiers in the rhizosphere of Plantago lanceolata growing in two contrasting sites. Plant Soil 91:377–380

    Article  Google Scholar 

  • Bowers MD, Collinge SK, Gamble SE, Schmitt J (1992) Effects of genotype, habitat, and seasonal variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia 91:201–207

    Article  Google Scholar 

  • Bowers MD, Stamp NE (1992) Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J Chem Ecol 18:985–995

    Article  CAS  Google Scholar 

  • Cassman KG, Dobermann A, Walters DT (2002) Agroecosystems, nitrogen use efficiency, and nitrogen management. Ambio 31:132–140

    PubMed  Google Scholar 

  • Davini E, Iavarone C, Trogolo C, Aureli P, Pasolini B (1986) The quantitative isolation and antimicrobial activity of the aglycone of aucubin. Phytochemistry 25:2420–2422

    Article  CAS  Google Scholar 

  • Dinnes DL, Karlen DL, Jaynes DB, Kaspar TC, Hatfield JL, Colvin TS, Cambardella CA (2002) Nitrogen management strategies to reduce nitrate leaching in tile-drained Midwestern soils. Agron J 94:153–171

    Article  Google Scholar 

  • Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33:855–869

    Article  PubMed  CAS  Google Scholar 

  • Fillery IRP (2007) Plant-based manipulation of nitrification in soil: a new approach to managing N loss. Plant Soil 294:1–4

    Article  CAS  Google Scholar 

  • Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843

    Article  PubMed  CAS  Google Scholar 

  • Gilch S, Meyer O, Schmidt I (2010) Electron paramagnetic studies of the copper and iron containing soluble ammonia monooxygenase from Nitrosomonas europaea. Biometals 23:613–622

    Article  PubMed  CAS  Google Scholar 

  • Gonda S, Tóth L, Gyémánt G, Braun M, Emrid T, Vasasa G (2012) Effect of high relative humidity on dried Plantago lanceolata L. leaves during long term storage: effects on chemical composition, colour and microbiological quality. Phytochem Anal 23:88–93

    Article  PubMed  CAS  Google Scholar 

  • Gopalakrishnan S, Watanabe T, Pearse SJ, Ito O, Hossain ZA, Subbarao GV (2009) Biological nitrification inhibition by Brachiaria humidicola roots varies with soil type and inhibits nitrifying bacteria, but not other major soil microorganisms. Soil Sci Plant Nutr 55:725–733

    Article  CAS  Google Scholar 

  • Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243

    Article  PubMed  Google Scholar 

  • Handjieva N, Mitova M, Ancev M, Popov S (1996) Iridoid glycosides from Gallium album and G. lovcense. Phytochemistry 43:625–628

    Article  CAS  Google Scholar 

  • Herbert JM, Maffrand JP, Taoubi K, Augereau JM, Fouraste I, Gleye J (1991) Verbascoside isolated from Lantana camara, an inhibitor of protein kinase C. J Nat Prod 54:1595–1600

    Article  PubMed  CAS  Google Scholar 

  • Hooper AB, Terry KR (1973) Specific inhibitors of ammonia oxidation in Nitrosomonas. J Bacteriol 115:480–485

    PubMed  CAS  Google Scholar 

  • Hyman MR, Arp DJ (1992) 14C2H2 and 14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J Biol Chem 267:1534–1545

    PubMed  CAS  Google Scholar 

  • Jensen ES (1994) Mineralization–immobilization of nitrogen in soil amended with low C:N ratio plant residues with different particle sizes. Soil Biol Biochem 26:519–521

    Article  Google Scholar 

  • Jensen ES (1997) Nitrogen immobilization and mineralization during initial decomposition of 15N-labelled pea and barley residues. Biol Fertil Soils 24:39–44

    Article  CAS  Google Scholar 

  • Kelly JJ, Policht K, Grancharova T, Lakhwinder SH (2011) Distinct responses in ammonia-oxidizing archaea and bacteria after addition of biosolids to an agricultural soil. Appl Environ Microbiol 77:6551–6558

    Article  PubMed  CAS  Google Scholar 

  • Kim DH, Kim BR, Kim JY, Jeong YC (2000) Mechanism of covalent adduct formation of aucubin to proteins. Tox Lett 114:181–188

    Article  CAS  Google Scholar 

  • Kowalchuk GA, Stienstra AW, Heilig SJR, Woldendorp JW (2000) Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ Microbiol 2:99–110

    Article  PubMed  CAS  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, QiJ NGW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  PubMed  CAS  Google Scholar 

  • LfULG—Sächsisches Landesamt für Umwelt, Landwirtschaft und Geologie. Online Meterological Database: Weather Station: Pillnitz-Versuchsstation (PIL). Available at http://www.landwirtschaft.sachsen.de/Wetter. Accessed 26 Jan 2012

  • Macías FA, Molinillo JM, Varela RM, Galindo JC (2007) Allelopathy—a natural alternative for weed control. Pest Manag Sci 63:327–348

    Article  PubMed  Google Scholar 

  • Nieder R, Benbi DK, Scherer HW (2011) Fixation and defixation of ammonium in soils: a review. Biol Fertil Soils 47:1–14

    Article  CAS  Google Scholar 

  • Nygaard Sorensen J, Thorup-Kristensen K (2011) Plant-based fertilizers for organic vegetable production. J Plant Nutr Soil Sci 174:321–332

    Article  Google Scholar 

  • Paavolainen L, Kitunen V, Smolander A (1998) Inhibition of nitrification in forest soil by monoterpenes. Plant Soil 205:147–154

    Article  CAS  Google Scholar 

  • Pankoke H, Bowers MD, Dobler S (2010) Influence of iridoid glycoside containing host plants on midgut β-glucosidase activity in a polyphagous caterpillar, Spilosoma virginica Fabricius (Arctiidae). J Insect Physiol 56:1907–1912

    Article  PubMed  CAS  Google Scholar 

  • Pardo F, Perich F, Villarroel L, Torres R (1993) Isolation of verbascoside, an antimicrobial constituent of Buddleja globosa leaves. J Ethnopharm 39:221–222

    Article  CAS  Google Scholar 

  • Prosser JI (2007) The ecology of nitrifying bacteria. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 223–243

    Chapter  Google Scholar 

  • Qin S, Hu C, Dong W (2010) Nitrification results in underestimation of soil urease activity as determined by ammonium production rate. Pedobiologica 53:401–404

    Article  CAS  Google Scholar 

  • Rauber R, Liebenau S, Friedrichs E, Schmidtke K (2008) Agronomic effects of underseeding ribwort plantain (Plantago lanceolata L.) in organically grown potatoes. Pflanzenbauwiss 12:32–40

    Google Scholar 

  • Reigosa MJ, Souto XC, Gonzalez L (1999) Effect of phenolic compounds on the germination of six weeds species. Plant Growth Regul 28:83–89

    Article  CAS  Google Scholar 

  • Rice EL (1984) Allelopathy. Physiological ecology. A series of monographs, texts and treatises, 2nd edn. Academic, Orlando

    Google Scholar 

  • Ritz K, Griffiths BS (1987) Effects of carbon and nitrate additions to soil upon leaching of nitrate, microbial predators and nitrogen uptake by plants. Plant Soil 102:229–237

    Article  CAS  Google Scholar 

  • SAS Institute (2011) Statistical analysis system, release 9.3. SAS Institute, Cary

  • Schuster M, Conrad R (1992) Metabolism of nitric-oxide and nitrous-oxide during nitrification and denitrification in soil at different incubation conditions. FEMS Microbiol Ecol 101:133–143

    CAS  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Google Scholar 

  • Singh HP, Batish DR, Kohli RK (2008) Allelopathy in agroecosystems. J Crop Prod 4:1–41

    Article  Google Scholar 

  • Skiba MW, George TS, Baggs EM, Daniell TJ (2011) Plant influence on nitrification. Biochem Soc Trans 39:275–278

    Article  PubMed  CAS  Google Scholar 

  • Smolander A, Kanerva S, Adamczyk B, Kitunen V (2012) Nitrogen transformations in boreal forest soils—does composition of plant secondary compounds give any explanations. Plant Soil 350:1–26

    Article  CAS  Google Scholar 

  • Štursová M, Baldrian P (2010) Effects of soil properties and management on the activity of soil organic matter transforming enzymes and the quantification of soil-bound and free activity. Plant Soil 338:99–110

    Article  Google Scholar 

  • Subbarao GV, Ito O, Sahrawat KL, Berry WL, Nakahara K, Ishikawa T, Watanabe T, Suenaga K, Rondon M, Rao IM (2006) Scope and strategies for regulation of nitrification in agricultural systems—challenges and opportunities. Crit Rev Plant Sci 25:1–33

    Article  Google Scholar 

  • Subbarao GV, Rondon M, Ito O, Ishikawa T, Rao IM, Nakahara K, Lascano C, Berry WL (2007a) Biological nitrification inhibition (BNI)—is it a widespread phenomenon. Plant Soil 294:5–18

    Article  CAS  Google Scholar 

  • Subbarao GV, Wang HY, Ito O, Nakahara K, Berry WL (2007b) NH4 + triggers the synthesis and release of biological nitrification inhibition compounds in Brachiaria humidicola roots. Plant Soil 290:245–257

    Article  CAS  Google Scholar 

  • Sunar S, Aksakal O, Yildirim N, Agar G (2009) Determination of the genotoxic effects of Verbascum speciosum Schrad. extracts on corn (Zea mays L.) seeds. Rom Biotechnol Lett 14:4820–4826

    Google Scholar 

  • Tamura Y, Nishibe S (2002) Changes in the concentrations of bioactive compounds in plantain leaves. J Agr Food Chem 50:2514–2518

    Article  CAS  Google Scholar 

  • Taskova R, Kokubun T, Alipieva K (2011) HPLC of iridoids. In: Waksmundzka-Hajnos M, Sherma J (eds) High performance liquid chromatography in phytochemical analysis, no. 102. CRC, Boca Raton, pp 709–727

  • Veresoglou SD, Sen R, Mamolos AP, Veresoglou DS (2011) Plant species identity and arbuscular mycorrhizal status modulate potential nitrification rates in nitrogen-limited grassland soils. J Ecol 99:1339–1349

    Article  CAS  Google Scholar 

  • Wang T, Gui M, Liu H, Zhao H, Xu L, Zha M, Li J (2010) Secretion of catalpol from Rehmannia glutinosa roots to the rhizosphere. Acta Physiol Plant 132:141–144

    Article  Google Scholar 

  • Ward BB, Courtney KJ, Langenheim JH (1997) Inhibition of Nitrosomonas europaea by monoterpenes from coastal redwood (Sequoia sempervirens) in whole-cell studies. J Chem Ecol 23:2583–2598

    Article  CAS  Google Scholar 

  • Wheatley RE, Ritz K, Griffiths BS (1997) Application of an augmented nitrification assay to elucidate the effects of a spring barley crop and manures on temporal variations in rates. Biol Fert Soils 24:378–383

    Article  CAS  Google Scholar 

  • White CS (1994) Monoterpenes—their effects on ecosystem nutrient cycling. J Chem Ecol 20:1381–1406

    Article  CAS  Google Scholar 

  • Wichtl M (2004) Herbal drugs and phytopharmaceuticals, 3rd edn. CRC, Boca Raton

  • Wurst S, Waagenar R, Biere A, van der Putten WH (2010) Microorganisms and nematodes increase levels of secondary metabolites in roots and root exudates of Plantago lanceolata. Plant Soil 329:117–126

    Article  CAS  Google Scholar 

  • You J, Das A, Dolan EM, Hu Z (2009) Ammonia-oxidizing archaea involved in nitrogen removal. Water Res 43:1801–1809

    Article  PubMed  CAS  Google Scholar 

  • Zubair M, Nybom H, Lindholm C, Rumpunen K (2011) Major polyphenols in aerial organs of greater plantain (Plantago major L.), and effects of drying temperature on polyphenol contents in the leaves. Sci Hortic-Amsterdam 128:523–529

    Article  CAS  Google Scholar 

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Acknowledgments

We thank E. Brunner for the pleasant cooperation. Furthermore, we acknowledge all analysts from BFUL Leipzig. Special thanks go to S. Unsicker, J. Gaugler, D. Bechtel, M. Krause, and C.v. Verschuer for the support of this study.

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Dietz, M., Machill, S., Hoffmann, H.C. et al. Inhibitory effects of Plantago lanceolata L. on soil N mineralization. Plant Soil 368, 445–458 (2013). https://doi.org/10.1007/s11104-012-1524-9

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