Abstract
Background and aims
Besides general effect of organic residues on soil quality and plant crop, hormonal direct effect on plant growth by extracted humic acids of organic materials is interesting and profitable theme. In the present work, we studied on direct interaction between humic acid and root growth, depending on different origin of organic materials.
Methods
All extracted humic acids of four organic materials (sewage sludge, compost sewage sludge, municipal solid waste, compost municipal solid waste) were characterized chemically by elemental analyses, ion pair chromatography (ICP), size exclusion chromatography (HPSEC), solid-state nuclear magnetic resonance (13C-CPMAS-NMR) and quantification of IAA. Later, different morphological effects on maize (principal root growth, lateral root growth, root area, root mitosic site, root dry weight and H+-ATPase activity of plasma membrane) were analyzed.
Results
All humic acids samples promoted root growth and proton pump activity in maize vesicles, especially those composted samples, which contained more carboxylic groups and had a more hydrophobic character, produced preferentially morphological and biochemical effects.
Conclusion
The conformational dynamics of humic hydrophobic associations in the rhizosphere may release auxin-like plant growth promoters and enhance plant biochemical activities. These organic wastes represent a renewable source of humic acid for use as plant root promoter.
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References
Adani F, Genevini P, Zacchero P, Zocchi G (1998) The effect of commercial humic acid on tomato plant growth and mineral nutrition. J Plant Nutr 21:561–575
Aguirre E, Leménager D, Bacaicoa E, Fuentes M, Baigorri R, Zamarreño AM, García Mina JM (2009) The root application of a purified leonardite humic acid modifies that transcriptional regulation of the main physiological root responses to Fe deficiency in Fe-sufficient cucumber plants. Plant Physiol Biochem 47:215–223
Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinised tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131
Bidegain RA, Kaemmerer M, Guiresse M, Hafidi M, Rey F, Morard P, Revel JC (2000) Effects of humic substances from composted or chemically decomposed poplar sawdust on mineral nutrition of ryegrass. J Agric Sci 134:259–267
Bottomley WB (1917) Some effects of organic growth-promotion substances (auximones) on the growth of Lemma minor in mineral cultural solutions. Proc R Soc Lon B Biol 89:481–505
Bouma TJ, Nilsen KL, Koutstaal B (2000) Sample preparation and scanning protocol for computerised analysis of root length and diameter. Plant Soil 218:185–196
Campitelli P, Ceppi S (2008) Chemical, physical and biological compost and vermicompost characterization: a chemometric study. Chemometr Intell Lab 90:64–71
Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR (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
Canellas LP, Zandonadi DB, Olivares FL, Façanha AR (2006) Efeitos fisiológicos de substâncias húmicas – o estímulo as H+-ATPases. In: Fernandes MS (ed) Nutrição Mineral de Plantas. Sociedade Brasileira de Ciência do Solo, Viçosa, pp 175–200
Canellas LP, Zandonadi DB, Busato JG, Baldotto MA, Simes ML, Martin-Neto L, Faanha AR, Spaccini R, Piccolo A (2008) Bioactivity and chemical characteristics of humic acids from tropical soils sequence. Soil Sci 173:624–637
Canellas LP, Spaccini R, Piccolo A, Dobbss LB, Okorokova-Façanha AL, Santos GDA, Olivares FL, Façanha AR (2009) Relationships between chemical characteristics and root gowth promotion of humic acids isolated from Brazilian oxisols. Soil Sci 174:611–620
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
Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inzé D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852
Chefetz B, Hatcher PG, Hadar Y, Chen Y (1996) Chemical and biological characterization of organic matter during composting of municipal solid waste. J Environ Qual 25:776–785
Chen Y, Clapp CE, Magen H (2004) Mechanisms of plant growth stimulation by humic substances: the role of organo iron complexes. Soil Sci Plant Nutr 50:1089–1095
Dobbss LB, Canellas LP, Olivares FL, Aguiar NO, Peres LEP, Azevedo M, Spaccini R, Piccolo A, Façanha AR (2010) Bioactivity of chemically transformed humic matter from vermicompost on plant root growth. J Agric Food Chem 58:3681–3688
Dobrev PI, Kamínek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr 950:21–29
Eyheraguibel B, Silvestre J, 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
González-Vila FJ, Almendros G, Madrid F (1999) Molecular alterations of organic fractions from urban waste in the course of composting and their further transformations in amended soils. Sci Total Environ 236:215–229
Guminski S (1968) Present-day views on physiological effects induced in plant organism by humic compounds. Sov Soil Sci+ 1250–1256
Hager A, Debus G, Edel HG, Stransky H, Serrano R (1991) Auxin induces exocytosis and the rapid synthesis of a high-turnover pool of plasma-membrane H+-ATPase. Planta 185:527–537
Hatcher PG, Nanny MA, Minard RD, Dible SD, Carson DM (1995) Comparison of two thermochemolytic methods for the analysis of lignin in decomposing gymnosperm wood: the CuO oxidation method and the method of thermochemolysis with tetramethylammonium hydroxide (TMAH). Org Geochem 23:881–888
Inbar Y, Chen Y, Hadar Y (1990) Characterization of humic substances formed during the composting of organic matter. Soil Sci Soc Am J 54:1316–1323
Jahn T, Baluska F, Michalke W, Harper JF, Volkmann D (1998) A membrane H+-ATPase in the root apex: evidence for strong expression in xylem parenchyma and asymmetric localization within cortical and epidermal cells. Physiol Plant 104:311–316
Khaled H, Fawy HA (2011) Effect of different levels of humic acids on the nutrient content, plant growth, and soil properties under conditions of salinity. Soil Water Res 6:21–29
Kogel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162
Magdoff F, Weil RR (2004) Soil organic matter in sustainable agriculture. CRC Press, Upper Saddle River
Moreno JL, **do K, Hernández T, García C (2007) Total and immobilized enzymatic activity of organic materials before and after composting. Compost Sci Util 15:93–100
Morsomme PM, Boutry M (2000) The plant plasma-membrane H+-ATPase: structure, function and regulation. Biochim Biophys Acta 1465:1–16
Muscolo A, Pannuccio MR, Abenavoli MR, Concheri G, Nardi S (1996) Effect of molecular complexity and acidity of earthworm faeces humic fractions on glutamate dehydrogenase, glutamine synthetase, and phosphoenolpyruvate carboxylase in Daucus carota α II cells. Biol Fertil Soils 22:83–88
Muscolo A, Cutrupi S, Nardi S (1998) IAA detection in humic substances. Soil Biol Biochem 30:1199–1201
Muscolo A, Sidari M, Francioso O, Tugnoli V, Nardi S (2007a) The auxin-like acitivity of humic substances is related to membran interatcitons in carrot cell cultures. J Chem Ecol 33:115–129
Muscolo A, Sidari M, Francioso O, Tugnoli V, Nardi S (2007b) Biological activity of humic substances is related to ther chemical structure. Soil Sci Soc Am J 71:75–85
Napier MR (2001) Models of auxin binding. J Plant Growth Regul 20:244–254
Napier MR (2004) Plant hormone binding sites. Ann Bot (London) 93:227–233
Nardi S, Pizzeghello D, Muscolo A, Vianello A (2002) Physiological effects of humic substances in higher plants. Soil Biol Biochem 34:1527–1537
O’Donnell RW (1973) The auxin-like effects of humic preparations from leonardite. Soil Sci 116:106–112
Piccolo A, Conte P, Cozzolino A (2001) Chromatographic and spectrophotometric properties of dissolved humic substances compared with macromolecular polymers. Soil Sci 166:174–185
Pinton R, Varanini Z, Vizzotto G, Maggioni A (1992) Soil humic substances affect transport properties of tonoplast vesicles isolated from oat roots. Plant Soil 142:203–210
Pinton R, Cesco S, Iacolettig G, Astolfi S, Varanini Z (1999) Modulation of NO −3 uptake by water-extractable humic substances: involvement of root plasma membrane H+-ATPase. Plant Soil 215:155–161
Pinton R, Varanini Z, Nannipieri P (2007) The rhizosphere: biochemistry and organic substances at the soil–plant interface, 2nd edn. CRC Press, Madison, p 447
Plaza C, Nogales R, Senesi N, Benitez E, Polo A (2008) Organic matter humification by vermicomposting of cattle manure alone and mixed with two-phase olive pomace. Bioresour Technol 99:5085–5089
Provenzano MR, Oliveira SC, Silva MRS, Senesi N (2001) Assessment of maturity degree of composts from domestic solid wastes by fluorescence and fourier transform infrared spectroscopies. J Agric Food Chem 49:5874–5879
Quaggiotti S, Ruperti B, Pizzeghello D, Francioso O, Tugnoli V, 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 55:803–813
Rubery PH (1981) Auxin receptors. Annu Rev Plant Physiol 32:569–596
Sánchez-Monedero MA, Cegarra J, García D, Roig A, Paredes C (2002a) Effects of HCl–HF purification treatment on chemical composition and structure of humic acids. Eur J Soil Sci 53:375–381
Sánchez-Monedero MA, Cegarra J, García D, Roig A (2002b) Chemical and structural evolution of humic acids during organic waste composting. Biodegradation 13:361–371
Spaccini R, Piccolo A, Haberhauer G, Gerzabek MH (2000) Transformation of organic matter from maize residues into labile and humic fractions of three European soils as revealed by 13C distribution and CPMAS-NMR spectra. Eur J Soil Sci 51:583–594
Spaccini R, Piccolo A (2009) Molecular characteristics of humic acids extracted from compost at increasing maturity stages. Soil Biol Biochem 41:1164-1172
Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions (2nd edn). Wiley
Sze H, Li X, Palmgren MG (1999) Energization of plant cell membranes by H+-pum** ATPases: regulation and biosynthesis. Plant Cell 11:677–689
Tan KH, Nopamornbodi V (1979) Effect of different levels of humic acids on nutrient content and growth of corn (Zea Mays L.). Plant Soil 51:283–287
Trevisan S, Pizzeghello D, Ruperti B, Francioso O, Sassi A, Palme K, Quaggiotti S, 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 Biol 12:604–614
Vaughan D, Malcolm RE (1985) Influence of humic substances on growth and physiological process. In: Vaughan D, Malcolm RE (eds) Soil organic matter and biological activity. Kluwer, Dordrecht, pp 77–108
Zandonadi DB, Canellas LP, Façanha AR (2007) Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+ pumps activation. Planta 225:1583–1595
Acknowledgments
This research was financially supported by CNPq (National Council for Scientific and Technological Development, Brazil), FAPERJ (Rio de Janeiro State Agency for Research) and the Spanish SENECA foundation.
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**do, K., Martim, S.A., Navarro, E.C. et al. Root growth promotion by humic acids from composted and non-composted urban organic wastes. Plant Soil 353, 209–220 (2012). https://doi.org/10.1007/s11104-011-1024-3
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DOI: https://doi.org/10.1007/s11104-011-1024-3