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Humic-like bioactivity on emergence and early growth of maize (Zea mays L.) of water-soluble lignins isolated from biomass for energy

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Abstract

Background and Aims

Lignin of lignocellulosic residues from biomass for energy can be exploited in sustainable agriculture as plant stimulants. Lignin monomers or their microbial bioproducts are mainly responsible for the plant growth promotion exerted by humic matter in soil. The aim of this work was to verify the humic-like bioactivity of water-soluble lignin isolated from biomass for energy towards plant growth and relate the biostimulation to the lignin molecular structure.

Methods

Two water-soluble lignins isolated from giant reed (AD) and miscanthus (MG) were characterized for molecular composition by 1H and 31P 1D-, 13C-1H 2D-, DOSY-NMR spectroscopy and for conformational structure by size-exclusion chromatography. The effect of different aqueous concentrations of lignin on germination of maize seeds and growth of maize plantlets was assessed in growth-chamber experiments.

Results

Both lignins showed humic-like supramolecular structures, but different conformational stability and molecular composition. Their largest bioactivity was revealed at 10 and 50 ppm of lignin organic carbon and both significantly increased length of radicles, lateral seminal roots, and coleoptiles of maize seedlings, as well as total shoot and root dry weights and root length of maize plantlets. However, differences in AD and MG bioactivity were attributed to their conformational stabilities and content of amphiphilic molecules, which may control both the adhesion to plant roots and the release of bioactive molecules upon interactions with plant-exuded organic acids.

Conclusions

The humic-like bioactivity of water-soluble lignins indicated that lignocellulosic residues from energy crops may be profitably recycled in agriculture as effective plant growth promoters, thereby increasing the economic and environmental sustainability of energy production from non-food biomasses.

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References

  • Al Chami Z, Alwanney D, De Pascali S, Cavoski I, Fanizzi F (2014) Extraction and characterization of bio-effectors from agro-food processing by-products as plant growth promoters. Chem Biol Technol Agric 1:17

    Article  Google Scholar 

  • Almaghrabi OA (2012) Control of wild oat (Avena fatua) using some phenolic compounds. Germination and some growth parameters. Saudi J Biol Sci 19:17–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bălaş A, Popa VI (2007) The influence of natural aromatic compounds on the development of Lycopersicon esculentum plantlets. BioResources 2:363–370

    Google Scholar 

  • Bayer C, Mielniczuk J, Amado TJC, Martin-Neto L, Fernandes SV (2000) Organic matter storage in a sandy clay loam Acrisol affected by tillage and cropping systems in southern Brazil. Soil Till Res 54:101–109

    Article  Google Scholar 

  • Canellas LP, Olivares FL (2014) Physiological responses to humic substances as plant growth promoter. Chem Biol Technol Agric 1:3

    Article  Google Scholar 

  • Canellas LP, Piccolo A, Dobbss LB, Spaccini R, Olivares FL, Zandonadi DB, Façanha AR (2010) Chemical composition and bioactivity properties of size-fractions separated from a vermicompost humic acid. Chemosphere 78:457–466

    Article  CAS  PubMed  Google Scholar 

  • Carvalho-Netto OV, Bressiani JA, Soriano HL, Fiori CS, Santos JM, Barbosa G, Xavier MA, Landell GAL, Pereira GAG (2014) The potential of the energy cane as the main biomass crop for the cellulosic industry. Chem Biol Technol Agric 1:20

    Article  Google Scholar 

  • Chaves N, Sosa T, Alìas JC, Escudero JC (2001) Identification and effect of interaction phytotoxic compounds from exudates of cistus ladanifer leaves. J Chem Ecol 27:611–621

    Article  CAS  PubMed  Google Scholar 

  • Chendev YG, Sauer TJ, Ramirez GH, Burras CL (2015) History of east European chernozem soil degradation; protection and restoration by tree windbreaks in the Russian steppe. Sustainability 7:705–724

    Article  CAS  Google Scholar 

  • Cherubini F (2010) The biorefinery concept: using biomass instead of oil for producing energy and chemicals. Energ Convers Manag 51:1412–1421

    Article  CAS  Google Scholar 

  • Crestini C, Argyropoulos DS (1997) Structural analysis of wheat straw lignin by quantitative 31P and 2D NMR Spectroscopy. The occurrence of ester bonds and α-O-4 substructures. J Agric Food Chem 45:1212–1219

    Article  CAS  Google Scholar 

  • Djurdjević L, Dinić A, Pavlović P, Mitrović M, Karadžić B, Tešević V (2004) Allelopathic potential of Allium ursinum L. Biochem Syst Ecol 32:533–544

    Article  Google Scholar 

  • du Jardin P (2012) The science of plant biostimulants-a bibliographic analysis. Contract 30-CE0455515/00-96, ad hoc Study on bio-stimulants products. Last access: 07/06/2015.http://ec.europa.eu/enterprise/sectors/chemicals/files/fertilizers/final_report_bio_2012_en.pdf.

  • Ertani A, Francioso O, Tugnoli V, Righi V, Nardi S (2011a) Effect of commercial lignosulfonate-humate on Zea mays metabolism. J Agric Food Chem 59:11940–11948

    Article  CAS  PubMed  Google Scholar 

  • Ertani A, Schiavon M, Altissimo A, Franceschi C, Nardi S (2011b) Phenol-containing organic substances stimulate phenylpropanoid metabolism in Zea mays. J Plant Nutr Soil Sci 174:496–503

    Article  CAS  Google Scholar 

  • Ertani A, Sambo P, Nicoletto C, Santagata S, Schiavon M, Nardi S (2015) The use of organic biostimulants in hot pepper plants to help low input sustainable agriculture. Chem Biol Technol Agric 2:11

    Article  Google Scholar 

  • Faix O, Meier D, Beinhoff O (1989) Analysis of lignocelluloses and lignins from Arundo donax L. and Miscanthus sinensis A., and hydroliquefaction of Miscanthus. Biomass 18:109–126

    Article  CAS  Google Scholar 

  • García AC, Santos LA, Izquierdo FG, Sperandio MV, Castro RN, Berbara RLL (2012) Vermicompost humic acids as an ecological pathway to protect rice plant against oxidative stress. Ecol Eng 47:203–208

    Article  Google Scholar 

  • Gerig T, Blum U (1991) Effects of mixtures of four phenolic acids on leaf area expansion of cucumber. J Chem Ecol 17:29–40

    Article  CAS  PubMed  Google Scholar 

  • González-García S, Hospido A, Agnemo R, Svensson P, Selling E, Moreira MT, Feijoo G (2001) Environmental life cycle assessment of a Swedish dissolving pulp mill integrated biorefinery. J Ind Ecol 15:568–583

    Article  Google Scholar 

  • Hatzakis E, Dagounakis G, Dais P (2010) A Facile NMR method for the quantification of total free and esterified sterols in virgin olive oil. Food Chem 122:346–352

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. California Agricultural Experimental Station Circular No. 347. University of California, Berkeley, pp 1–32

    Google Scholar 

  • Ibarra D, Chávez MI, Rencoret J, Del Río JC, Gutiérrez A, Romero J, Camarero S, Martínez MJ, Jiménez-Barbero J, Martínez AT (2007) Lignin Modification during Eucalyptus globulus Kraft pulping followed by totally chlorine-free bleaching: A two-dimensional nuclear magnetic resonance, fourier transform infrared, and pyrolysis − gas chromatography/mass spectrometry study. J Agric Food Chem 55:3477–3490

    Article  CAS  PubMed  Google Scholar 

  • Johnson CS Jr (1999) Diffusion ordered nuclear magnetic resonance spectroscopy: principles and applications. Prog Nucl Magn Reson Spectrosc 34:203–256

    Article  CAS  Google Scholar 

  • Kadla JK, Chang H, Jameel H (1999) The reactions of lignins with hydrogen peroxide at high temperature. Part 2. The oxidation of kraft lignin. Holzforschung 53:277–284

    Article  CAS  Google Scholar 

  • Kamble SV, Bhattacharyulu YC (2014) Soil conditioner by artificial ammoxidation of lignin and optimization using response surface methodology. Int J Innov Res Sci Eng Technol 3:16534–16539

    Article  Google Scholar 

  • Kesba HH, El-Betagi HS (2012) Biochemical changes in grape rootstocks resulted from humic acid treatments in relation to nematode infection. Asian Pac J Trop Biomed 2:287–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liebman M, Davis AS (2000) Integration of soil, crop and weed management in low-external-input farming systems. Weed Res 40:27–47

    Article  Google Scholar 

  • Lundquist K (1992) 1H NMR spectral studies of lignins. Nordic Pulp Pap Res J 1:8–16

    Google Scholar 

  • Nardi S, Pizzeghello D, Bragazza L, Gedol R (2003) Low-molecular-weight organic acids and hormone-like activity of dissolved organic matter in two forest soils in northern Italy. J Chem Ecol 29:1549–1564

    Article  CAS  PubMed  Google Scholar 

  • Nebbioso A, Mazzei P, Savy D (2014) Reduced complexity of multidimensional and diffusion NMR spectra of soil humic fractions as simplified by humeomics. Chem Biol Technol Agric 1:24

    Article  Google Scholar 

  • Nuzzo A, Piccolo A (2013) Oxidative and photo-oxidative polymerization of humic suprastructures by heterogeneous biomimetic catalysis. Biomacromolecules 14:1645–1652

    Article  CAS  PubMed  Google Scholar 

  • Pecha J, Fürst T, Kolomazník K, Friebrová V, Svoboda P (2011) Protein biostimulant foliar uptake modeling: the impact of climatic conditions. Fluid Mech Transp Phenom 58:2010–2019

    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 

  • Piccolo A, Nardi S, Concheri G (1996) Macromolecular changes of soil humic substances induced by interactions with organic acids. Eur J Soil Sci 47:319–328

    Article  CAS  Google Scholar 

  • Piccolo A, Conte P, Trivellone E, Van Lagen B, Buurman P (2002) Reduced heterogeneity of a lignite humic acid by preparative HPSEC following interaction with an organic acid. Characterization of size-separates by PYR-GC-MS and 1H-NMR spectroscopy. Environ Sci Technol 36:76–84

    Article  CAS  PubMed  Google Scholar 

  • Piccolo A, Conte P, Spaccini R, Chiarella M (2003) Effects of some dicarboxylic acids on the association of dissolved humic substances. Biol Fert Soils 37:255–259

    CAS  Google Scholar 

  • Pizzeghello D, Zanella A, Carletti P, Nardi S (2006) Chemical and biological characterization of dissolved organic matter from silver fir and beech forest soils. Chemosphere 65:190–200

    Article  CAS  PubMed  Google Scholar 

  • Popa V, Dumitru M, Volfa I, Anghel N (2008) Lignin and polyphenols as allelochemicals. Ind Crop Prod 27:144–149

    Article  CAS  Google Scholar 

  • Puglisi E, Fragoulis G, Ricciuti P, Cappa F, Spaccini R, Piccolo A, Trevisan M, Crecchio C (2009) Effects of a humic acid and its size-fractions on the bacterial community of soil rhizosphere under maize (Zea mays L.). Chemosphere 77:829–837

    Article  CAS  PubMed  Google Scholar 

  • Qiao J-Q, Wu H-J, Huo R, Gao X-W, Borriss R (2014) Stimulation of plant growth and biocontrol by Bacillus amyloliquefaciens subsp. plantarum FZB42 engineered for improved action. Chem Biol Technol Agric 1:12

    Article  Google Scholar 

  • Rasmussen JA, Einhellig FA (1977) Synergistic inhibitory effect of p-Coumaric and ferulic acids on germination and growth of grain sorghum. J Chem Ecol 3:197–205

    Article  CAS  Google Scholar 

  • Reigosa MJ, Souto XC, Gonzàlez L (1999) Effect of phenolic compounds on the germination of six weeds species. Plant Growth Regul 28:83–88

    Article  CAS  Google Scholar 

  • Rencoret J, Gutiérrez A, Nieto L, Jiménez-Barbero J, Faulds CB, Kim H, Ralph J, Martínez AT, del Río JC (2011) Lignin composition and structure in young versus adult eucalyptus globulus plants. Plant Physiol 155:667–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Restolho JA, Prates A, de Pinho MN, Afonso MD (2009) Sugars and lignosulphonates recovery from eucalyptus spent sulphite liquor by membrane processes. Biomass Bioenergy 33:1558–1566

    Article  CAS  Google Scholar 

  • Robert D (1992) The determination of lignin. In: Lin SY, Dence CW (eds) Methods in lignin chemistry. Springer-Verlag, Berlin, pp 250–2733

    Chapter  Google Scholar 

  • Savy D, Piccolo A (2014) Physical–chemical characteristics of lignins separated from biomasses for second-generation ethanol. Biomass Bioenergy 62:58–67

    Article  CAS  Google Scholar 

  • Savy D, Nebbioso A, Mazzei P, Drosos M, Piccolo A (2015a) Molecular composition of water-soluble lignins separated from different non-food biomasses. Fuel Process Technol 131:175–181

    Article  CAS  Google Scholar 

  • Savy D, Mazzei P, Roque R, Nuzzo A, Bowra S, Santos R (2015b) Structural recognition of lignin isolated from bioenergy crops by subcritical water: ethanol extraction. Fuel Process Technol. doi:10.1016/j.fuproc.2015.07.004

    Google Scholar 

  • Smejkalova D, Piccolo A (2008) Aggregation and disaggregation of humic supramolecular assemblies by NMR diffusion ordered spectroscopy (DOSY-NMR). Environ Sci Technol 42:699–706

    Article  CAS  PubMed  Google Scholar 

  • Tanase C, Boz I, Stingu A, Volf I, Popa VI (2014) Physiological and biochemical responses induced by spruce bark aqueous extract and deuterium depleted water with synergistic action in sunflower (Helianthus annuus L.) plants. Ind Crop Prod 60:160–167

    Article  CAS  Google Scholar 

  • Vaccaro S, Ertani A, Nebbioso A, Muscolo A, Quaggiotti S, Piccolo A, Nardi S (2015) Humic substances stimulate maize nitrogen assimilation and amino acid metabolism at physiological and molecular level. Chem Biol Technol Agric 2:5

    Article  Google Scholar 

  • Williams RD, Hoagland RE (1982) The effects of naturally occurring phenolic compounds on seed germination. Weed Sci 30:206–212

    CAS  Google Scholar 

  • You TT, Mao J, Yuan T, Wen JL, Xu F (2013) Structural elucidation of the lignins from stems and foliage of Arundo donax Linn. J Agric Food Chem 61:5361–5370

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was partially funded by the MIUR project PON01_01966/2 “ENERBIOCHEM”. The authors are grateful to the Institute of Biological Environmental and Rural Sciences (UK) for having provided the Miscanthus biomass.

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Correspondence to Alessandro Piccolo.

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Responsible Editor: Tim S. George.

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Savy, D., Cozzolino, V., Nebbioso, A. et al. Humic-like bioactivity on emergence and early growth of maize (Zea mays L.) of water-soluble lignins isolated from biomass for energy. Plant Soil 402, 221–233 (2016). https://doi.org/10.1007/s11104-015-2780-2

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