A simple technique for assessing the cuticular diffusion of humic acid biostimulants

Plant Methods - Tập 15 - Trang 1-11 - 2019
Marcela Smilkova1, Jiri Smilek2, Michal Kalina2, Martina Klucakova1, Miloslav Pekar1, Petr Sedlacek1
1Institute of Physical and Applied Chemistry, Brno University of Technology, Faculty of Chemistry, Brno, Czech Republic
2Materials Research Centre, Brno University of Technology, Faculty of Chemistry, Brno, Czech Republic

Tóm tắt

Experimental determination of the extent and rate of transport of liquid humates supplied to plants is critical in testing physiological effects of such biostimulants which are often supplied as foliar sprays. Therefore, an original experimental method for the qualitative investigation and quantitative description of the penetration of humates through plant cuticles is proposed, tested, and evaluated. The proposed method involves the isolation of model plant leaf cuticles and the subsequent in vitro evaluation of cuticular humate transport. The employed novel methodology is based on a simple diffusion couple arrangement involving continuous spectrophotometric determination of the amount of penetrated humate in a hydrogel diffusion medium. Prunus laurocerasus leaf cuticles were isolated by chemical and enzymatic treatment and the rate of cuticular penetration of a commercial humate (lignohumate) was estimated over time in quantitative and qualitative terms. Different rates of lignohumate transport were determined for abaxial and adaxial leaf cuticles also in relation to the different cuticular extraction methods tested. The proposed methodology represents a simple and cheap experimental tool for the study on the trans-cuticular penetration of humic-based biostimulants.

Tài liệu tham khảo

Neshev N, Manolov I. Content and uptake of nutrients with plant biomass of potatoes depending on potassium fertilization. Agric Agric Sci Procedia. 2015. https://doi.org/10.1016/j.aaspro.2015.08.039. Peigne J, Vian JF, Payet V, Saby NPA. Soil fertility after 10 years of conservation tillage in organic farming. Soil Tillage Res. 2018. https://doi.org/10.1016/j.still.2017.09.008. Okuda A, Kawasaki T, Yamada Y. Foliar absorption of nutrients. Soil Sci Plant Nutr. 1960. https://doi.org/10.1080/00380768.1960.10430928. Fernandez V, Eichert T. Uptake of hydrophilic solutes through plant leaves: current state of knowledge and perspectives of foliar fertilization. Crit Rev Plant Sci. 2009. https://doi.org/10.1080/07352680902743069. Fageria NK, Barbosa Filho MP, Moreira A, Guimaraes CM. Foliar fertilization of crop plants. J Plant Nutr. 2009. https://doi.org/10.1080/01904160902872826. Mandic V, Simic A, Krnjaja Z, Bijelic Z, Tomic A, Stanojkovic D, Ruzic Music D. Effect of foliar fertilization on soybean grain yield. Biotechnol Anim Husb. 2015. https://doi.org/10.2298/BAH1501133M. Li M, Wang S, Tian X, Li S, Chen Y, Jia Z, Liu K, Zhai A. Zinc and iron concentrations in grain milling fractions through combined foliar applications of Zn and macronutrients. Field Crop Res. 2016. https://doi.org/10.1016/j.fcr.2015.12.018. Chamel A, Gambonnet B. Sorption and diffusion of an ethoxylated stearic alcohol and an ethoxylated stearic amine into and through isolated plant cuticles. Chemosphere. 1997. https://doi.org/10.1016/S0045-6535(97)00033-7. Liu H, Shao B, Long X, Yao Y, Meng Q. Foliar penetration enhanced by biosurfactant rhamnolipid. Colloid Surf B. 2016. https://doi.org/10.1016/j.colsurfb.2016.05.058. Solel Z, Edgington LV. Transcuticular movement of fungicides. Phytophatology. 1972. https://doi.org/10.1094/Phyto-63-505. Chamel A, Vitton N. Sorption and diffusion of C14-atrazine through isolated plant cuticles. Chemosphere. 1996. https://doi.org/10.1016/0045-6535(96)00241-X. Wang CJ, Liu ZQ. Foliar uptake of pesticides—present status and future challenge. Pestic Biochem Phys. 2007. https://doi.org/10.1016/j.pestbp.2006.04.004. Zelena V, Veverka K. Effect of surfactants and liquid fertilizers on transcuticular penetration of fungicides. Plant Prot Sci. 2007. https://doi.org/10.17221/2236-PPS. Khayet M, Fernandez V. Estimation of the solubility parameters of model plant surfaces and agrochemicals: a valuable tool for understanding plant surface interactions. Theor Biol Med Model. 2012. https://doi.org/10.1186/1742-4682-9-45. Khorram MS, Zhang Q, Lin D, Zheng Y, Fang H, Yu Y. Biochar: a review of its impact on pesticide behavior in soil environments and its potential applications. J Environ Sci. 2016. https://doi.org/10.1016/j.jes.2015.12.027. Martin JT, Juniper BE. The cuticles of plants. New York: St. Martin’s Press; 1970. Riederer M, Schreiber L. Protecting against water loss: analysis of the barrier properties of plant cuticles. J Exp Bot. 2001. https://doi.org/10.1093/jexbot/52.363.2023. Barel D. Foliar application of phosphorus compounds. Doctoral thesis, Iowa State University, USA; 1975. p. 1–345. Villena JF, Dominguez E, Heredia A. Monitoring biopolymers present in plant cuticles by FT-IR. J Plant Physiol. 1999. https://doi.org/10.1016/S0176-1617(00)80083-8. Pollard M, Beisson F, Li Y, Ohlrogge JB. Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci. 2008. https://doi.org/10.1016/j.tplants.2008.03.003. Yeats TH, Rose JK. The formation and function of plant cuticles. Plant Physiol. 2013. https://doi.org/10.1104/pp.113.222737. Riederer M, Müller C. Biology of the plant cuticle. Annual plant reviews. Oxford: Blackwell; 2006. https://doi.org/10.1002/9780470988718. Gutschick VP. Biotic and abiotic consequences of differences in leaf structure. New Phytol. 1999. https://doi.org/10.1046/j.1469-8137.1999.00423.x. Zeisler-Diehl V, Migdal B, Schreiber L. Quantitative characterization of cuticular barrier properties: methods, requirements, and problems. J Exp Bot. 2017. https://doi.org/10.1093/jxb/erx282. Orgell WH. The isolation of plant cuticle with pectic enzymes. Plant Physiol. 1955;30:78–80. Holloway PJ, Baker EA. Isolation of plant cuticles with zinc chloride-hydrochloric acid solution (short communication). Plant Physiol. 1968. https://doi.org/10.1104/pp.43.11.1878. Solel Z. The systematic fungicidal effect of benzimidazole derivatives and thiophanate against Cercospora leaf spot of sugar beet. Phytopathology. 1970. https://doi.org/10.1094/Phyto-60-1186. Edgington LV, Buchenauer H, Grossmann F. Bioassay and transcuticular movement of systematic fungicides. Pestic Sci. 1973. https://doi.org/10.1002/ps.2780040517. Schonherr J, Lendzian K. A simple and inexpensive method of measuring water permeability of isolated plant cuticular membranes. Z Pflanzenphysiol. 1981. https://doi.org/10.1016/S0044-328X(81)80203-6. Yamada Y, Wittwer SH, Bukovac MJ. Penetration of organic compounds through isolated cuticular membranes with special reference to C14 urea. Plant Physiol. 1964. https://doi.org/10.1104/pp.40.1.170. Darlington WA, Cirulis N. Permeability of apricot leaf cuticle. Plant Physiol. 1963. https://doi.org/10.1104/pp.38.4.462. Wittwer SH, Lundahl WS. Autoradiography as an acid in determining the grass absorption and utilization of foliar applied nutrients. Plant Physiol. 1951;26:792–7. Eggert R, Kardos LT, Smith RD. The relative absorption of phosphorus by apple trees from foliar sprays and from soil applications of fertilizer using radioactive tracers. Proc Am Soc Hortic Sci. 1952;60:75–86. Tukey HB, Ticknor RL, Hinsvark ON, Wittwer SH. Absorption of nutrients by stems and branches of woody plants. Science. 1952. https://doi.org/10.1126/science.116.3007.167. Bargel H, Koch K, Cerman Z, Neinhuis Ch. Structure-function relationships of the plant cuticle and cuticular waxes—a smart material? Funct Plant Biol. 2006. https://doi.org/10.1071/FP06139. Bukovac MH, Wittwer SH. Absorption and mobility of foliar applied nutrients. Plant Physiol. 1957. https://doi.org/10.1104/pp.32.5.428. Yamada Y, Wittwer SH, Bukovac MJ. Penetration of ions through isolated cuticles. Plant Physiol. 1963. https://doi.org/10.1104/pp.39.1.28. Yu JH, Lim HK, Choi GJ, Cho KY, Kim JH. A new method for assessing foliar uptake of fungicides using Congo Red as a tracer. Pest Manag Sci. 2001. https://doi.org/10.1002/ps.327. Pinton R, Cesco S, Santi S, Varanini Z. Soil humic substances stimulate proton release by intact oat seedling roots. J Plant Nutr. 1997. https://doi.org/10.1080/01904169709365301. Chen Y, Clapp CE, Magen H, Cline VW. Stimulation of plant growth by humic substances: effects on iron availability. In: Ghabbour EA, Davies G, editors. Understanding humic substances: advanced methods, properties and applications. Cambridge: Royal Society of Chemistry; 1999. Russo RO, Berlyn GP. The use of organic biostimulants to help low input sustainable agriculture. J Sustain Agric. 1990. https://doi.org/10.1300/J064v01n02_04. Tan KH. Humic matter in soil and the environment. 2nd ed. New York: Marcel Dekker; 2003. Nardi S, Condheri G, Dell’Agnola G. Biological activity of humus. In: Piccolo A, editor. Humic substances in terrestrial ecosystems. Amsterdam: Elsevier; 1996. p. 361–406. Canellas LP, Olivares FL. Physiological responses to humic substances as plant growth promoter. Chem Biol Technol Agric. 2014. https://doi.org/10.1186/2196-5641-1-3. Nardi S, Pizzeghello D, Schiavon M, Ertani A. Plant biostimulants: physiological responses induced by protein hydrolyzed-based products and humic substances in plant metabolism. Sci Agric. 2016. https://doi.org/10.1590/0103-9016-2015-0006. Tejada M, Gonzalez JL. Influence of foliar fertilization with amino acids and humic acids on productivity and quality of asparagus. Biol Agric Hortic. 2003. https://doi.org/10.1080/01448765.2003.9755270. Pizzeghello D, Nicolini G, Nardi S. Hormone-like activity of humic substances in Fagus sylvaticae forests. New Phytol. 2001. https://doi.org/10.1046/j.0028-646x.2001.00223.x. Basiolio ZD, Pasqualoto CL, Facanha AR. Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+ pumps activation. Planta. 2007. https://doi.org/10.1007/s00425-006-0454-2. Jackson TA. Effects of clay minerals, oxyhydroxides, and humic matter on microbial communities of soil, sediment, and water. In: Huang PH, et al., editors. Environmental impact of soil component interactions: metals, inorganics and microbial activity. Berlin Heidelberg: CRC Press, Springer; 1995. p. 165–200. Parandian F, Samavat S. Effects of fulvic and humic acid on anthocyanin, soluble sugar, α-amylase enzyme and some micronutrient elements in Lilium. Int Res J Appl Basic Sci. 2012;3:924–9. Dorer SP, Peacock CH. The effect of humate and organic fertilizer on establishment and nutrient of creeping bent putting greens. Int Turfgrass Soc. 1997;78:437–43. Liu C, Cooper RJ, Bowman DC. Humic acid application affects photosynthesis, root development, and nutrient content of creeping bentgrass. HortScience. 1998;33:1023–5. Fernandez-Escobar R, Benlloch M. Response of olive trees to foliar application of humic substances extracted from leonardite. Sci Hortic. 1996. https://doi.org/10.1016/S0304-4238(96)00914-4. Maibodi NDH, Kafi M, Nikbakht A, Rejali F. Effect of foliar applications of humic acid on growth, visual quality, nutrients content and root parameters of perennial ryegrass (Lolium perenne L.). J Plant Nutr. 2014. https://doi.org/10.1080/01904167.2014.939759. Bettoni MM, Mogor AF, Pauletti V, Goicoechea N, Aranjuelo I, Germendia I. Nutritional quality and yield of onion as affected by different application methods and doses of humic substances. J Food Compos Anal. 2016. https://doi.org/10.1016/j.jfca.2016.06.008. Olk DC, Dinnes DL, Rene Scoresby J, Callaway CR, Darlington JW. Humic products in agriculture: potential benefits and research challenges–a review. J Soils Sediments. 2018. https://doi.org/10.1007/s11368-018-1916-4. Rose MT, Patti AF, Little KR, Brown AL, Roy Jackson W, Cavagnaro TR. A meta-analysis and review of plant-growth response to humic substances: practical implications for agriculture. Adv Agron. 2014. https://doi.org/10.1016/B978-0-12-800138-7.00002-4. Lyons G, Genc Y. Commercial humates in agriculture: real substance or smoke and mirrors? Agronomy. 2016. https://doi.org/10.3390/agronomy6040050. Kulikova NA, Abroskin DP, Badun G, Chernysheva MG, Korobkov VI, Beer AS, Tsvetkova EA, Senik SV, Klein OI, Perminova IV. Label distribution in tissues of wheat seedlings cultivated with tritium-labeled leonardite humic acid. Sci Rep. 2016. https://doi.org/10.1038/srep28869. Sedlacek P, Smilek J, Klucakova M. How the interactions with humic acids affect the mobility of ionic dyes in hydrogels—2. Non-stationary diffusion experiments. React Funct Polym. 2014. https://doi.org/10.1016/j.reactfunctpolym.2013.12.002. Smilek J, Sedlacek P, Klucakova M. On the role of humic acids’ carboxyl groups in the binding of charged organic compounds. Chemosphere. 2015. https://doi.org/10.1016/j.chemosphere.2015.06.093. Gladkov OA. U.S. Patent 7198805B2, Method for producing humic acid salts, Sankt-Peterburg (RU), chemical abstract (57). 2007. Novak F, Sestauberova M, Hrabal R. Structural features of lignohumic acids. J Mol Struct. 2015. https://doi.org/10.1016/j.molstruc.2015.03.054. Sedlacek P, Smilek J, Klucakova M. How the interactions with humic acids affect the mobility of ionic dyes in hydrogels—results from diffusion cells. React Funct Polym. 2013. https://doi.org/10.1016/j.reactfunctpolym.2013.07.008. Sedlacek P, Smilek J, Kalina M, Lastuvkova M, Klucakova M. Hydrogels: invaluable experimental tool for demonstrating diffusion phenomena in physical chemistry laboratory courses. J Mater Educ. 2017;39:59–90. Smilek J, Sedlacek P, Lastuvkova M, Kalina M, Klucakova M. Transport of organic compounds through porous systems containing humic acids. Bull Environ Contam Toxicol. 2017. https://doi.org/10.1007/s00128-016-1926-0. Cussler EL. Diffusion: mass transfer in fluid systems. 2nd ed. London: Cambridge University Press; 1997. Enev V, Pospisilova L, Klucakova M, Liptaj T, Doskocil L. Spectral characterization of selected humic substances. Soil Water Res. 2014. https://doi.org/10.17221/39/2013-SWR. Prochazka P, Stranc P, Pzderu K, Strnc J, Jedlickova M. The possibilities of increasing the production abilities of soya vegetation by seed treatment with biologically active compounds. Plant Soil Environ. 2015. https://doi.org/10.17221/225/2015-PSE. Prochazka P, Stranc P, Pazderu K, Stranc J. The influence of pre-sowing seed treatment by biologically active compounds on soybean seed quality and yield. Plant Soil Environ. 2016. https://doi.org/10.17221/570/2016-PSE. Crank J. The mathematics of diffusion. 2nd ed. Oxford: Clarendon Press; 1956. Guzman P, Fernandez V, Khayet M, Garcia ML, Fernandez A, Gil L. Ultrastructure of plant lead cuticles in relation to sample preparation as observed transmission electron microscopy. Sci World J. 2014. https://doi.org/10.1155/2014/963921. Tyree MT, Scherbatskoy D, Tabor CA. Leaf cuticles behave as asymmetric membranes: evidence from the measurement of diffusion potentials. Plant Physiol. 1990. https://doi.org/10.1104/pp.92.1.103. Guzman P, Fernandez V, Garcia ML, Khayet M, Fernandez A, Gil L. Localization of polysaccharides in isolated and intact cuticles of eucalypt, poplar and pear leaves by enzyme-gold labelling. Plant Physiol Biochem. 2014. https://doi.org/10.1016/j.plaphy.2013.12.023. Guzman P, Fernandez V, Garcia J, Cabral V, Hayali N, Khayet M, Gil L. Chemical and structural analysis of Eucalyptus globulus and E. camaldulensis leaf cuticles: a lipidized cell wall region. Front Plant Sci. 2014. https://doi.org/10.3389/fpls.2014.00481. Fernandez V, Guzman-Delgado P, Graca J, Santos S, Gil L. Cuticles structure in relation to chemical composition: re-assessing the prevailing model. Front Plant Sci. 2016. https://doi.org/10.3389/fpls.2016.00427. Riederer M, Schönherr J. Accumulation and transport of (2,4-dichlorophenoxy)acetic acid in plant cuticles. 1. Sorption in the cuticular membrane and its components. Ecotoxicol Environ Saf. 1984. https://doi.org/10.1016/0147-6513(85)90022-3. Eichert T, Burkhardt J. Quantification of stomatal uptake of ionic solutes using a new model system. J Exp Bot. 2001. https://doi.org/10.1093/jexbot/52.357.771. Burkhardt J, Basi S, Pariyar S, Hunsche M. Stomatal penetration by aqueous solutions—an update involving leaf surface particles. New Phytol. 2012. https://doi.org/10.1111/j.1469-8137.2012.04307.x. Schreiber L, Schonherr J. Water and solute permeability of plant cuticles. 1st ed. Berlin: Springer; 2009.