Abstract
In the current study, effects of chitosan oligomers (CHI-OM) with different polymerization degrees (DP) between 2 and 15, and polymeric chitosan (CHI-P) with a DP of 70 were compared with kinetin (KIN), 6-benzylaminopurine (BAP), indole-3-butyric acid (IBA), indole-3-acetic acid (IAA), and jasmonic acid (JAS) on the structure and composition of several biomolecules in the root system of Serapias vomeracea. Evaluation of molecular alterations in the root system of S. vomeracea through an infrared spectroscopic approach provided insight into the differentiation between action mechanisms of chitosan and commonly used plant growth regulators. The results revealed that CHI-P and JAS treatments at low concentrations might enhance the lignin content in the cell walls. Also, JAS, CHI-OM, and CHI-P treatments enhanced cell wall lignification. The water-associated cellulose content of the cell walls was affected by the DP of chitosan. Membrane lipid stabilization and protein content were enhanced after CHI-P, JAS, and KIN treatments, while BAP and CHI-OM treatments triggered lipid, protein, and cell wall polysaccharide synthesis. In particular, CHI-OM treatment also enhanced rhamnogalacturonan and β-galactan content as well as xyloglucans and glucomannans, while the auxin treatments had a similar impact only on glucomannan content. These findings suggest that chitosan may show either purine-based cytokinin-like or lipid-based jasmonic acid-like activity in the root system of S. vomeracea. Additionally, depending on its degree of polymerization, the effects of chitosan may vary on root system development in S. vomeracea.
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References
Acemi A (2020a) Polymerization degree of chitosan affects structural and compositional changes in the cell walls, membrane lipids, and proteins in the leaves of Ipomoea purpurea: an FT-IR spectroscopy study. Int J Biol Macromol 162:715–722. https://doi.org/10.1016/j.ijbiomac.2020.06.171
Acemi A (2020b) Chitosan versus plant growth regulators: a comparative analysis of their effects on in vitro development of Serapias vomeracea (Burm.f.) Briq. Plant Cell Tiss Organ Cult 141:327–338. https://doi.org/10.1007/s11240-020-01789-3
Acemi A, Özen F (2019) Optimization of in vitro asymbiotic seed germination protocol for Serapias vomeracea. EuroBiotech J 3(3):143–151. https://doi.org/10.2478/ebtj-2019-0017
Acemi A, Türker-Kaya S, Özen F (2016) FT-IR spectroscopy based evaluation of changes in primary metabolites of Amsonia orientalis after in vitro 6-benzylaminopurine treatment. Not Bot Hort Agrobot 44(1):209–214. https://doi.org/10.15835/nbha44110194
Acemi A, Bayrak B, Çakır M, Demiryürek E, Gün E, El Gueddari NE, Özen F (2018) Comparative analysis of the effects of chitosan and common plant growth regulators on in vitro propagation of Ipomoea purpurea (L.) Roth from nodal explants. In Vitro Cell Dev Biol Plant 54:537–544. https://doi.org/10.1007/s11627-018-9915-0
Acemi A, Çobanoğlu Ö, Türker-Kaya S (2019) FT-IR-based comparative analysis of glucomannan contents in some tuberous orchids, and effects of pre-processing on glucomannan measurement. J Sci Food Agric 99:3681–3686. https://doi.org/10.1002/jsfa.9596
Akkas SB, Inci S, Zorlu F, Severcan F (2007) Melatonin affects the order, dynamics and hydration of brain membrane lipids. J Mol Struct 834–836:207–215. https://doi.org/10.1016/j.molstruc.2006.12.018
Asghari-Zakaria R, Maleki-Zanjani B, Sedghi E (2009) Effect of in vitro chitosan application on growth and minituber yield of Solanum tuberosum L. Plant Soil Environ 55(6):252–256
Baluška F, Mancuso S, Volkmann D, Barlow PW (2010) Root apex transition zone: a signalling–response nexus in the root. Trends Plant Sci 15:402–408. https://doi.org/10.1016/j.tplants.2010.04.007
Bellusci F, Pellegrino G, Musacchio A (2009) Different levels of inbreeding depression between outcrossing and selfing Serapias species (Orchidaceae). Biol Plant 53:175–178. https://doi.org/10.1007/s10535-009-0029-8
Boggs JM (1987) Lipid intermolecular hydrogen bonding: influence on structural organization and membrane function. Biochim Biophys Acta 906(3):353–404. https://doi.org/10.1016/0304-4157(87)90017-7
Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25:162–172. https://doi.org/10.1016/j.pbi.2015.05.014
Couchoud M, Der C, Girodet S, Vernoud V, Prudent M, Leborgne-Castel N (2019) Drought stress stimulates endocytosis and modifies membrane lipid order of rhizodermal cells of Medicago truncatula in a genotype-dependent manner. BMC Plant Biol 19:22. https://doi.org/10.1186/s12870-019-1814-y
Das SN, Madhuprakash J, Sarma PVSRN, Purushotham P, Suma K, Manjeet K, Rambabu S, El Gueddari NE, Moerschbacher BM, Podile AR (2015) Biotechnological approaches for field applications of chitooligosaccharides (COS) to induce innate immunity in plants. Crit Rev Biotechnol 35(1):29–43. https://doi.org/10.3109/07388551.2013.798255
Dokken KM, Davis LC (2007) Infrared imaging of sunflower and maize root anatomy. J Agric Food Chem 55(26):10517–10530. https://doi.org/10.1021/jf072052e
Ellis DI, Goodacre R (2006) Metabolic fingerprinting in disease diagnosis: biomedical applications of infrared and Raman spectroscopy. Analyst 131(8):875–885. https://doi.org/10.1039/b602376m
Fabian H, Naumann D (2012) Millisecond-to-minute protein folding/misfolding events monitored by FT-IR spectroscopy. In: Fabian H, Naumann D (eds) Protein folding and misfolding. Springer, Germany, pp 53–89. https://doi.org/10.1007/978-3-642-22230-6_3
Galichet A, Sockalingum G, Belarbi A, Manfait M (2001) FT-IR spectroscopic analysis of Saccharomyces cerevisiae cell walls: study of an anomalous strain exhibiting a pink-colored cell phenotype. FEMS Microbiol Lett 197:179–186. https://doi.org/10.1111/j.1574-6968.2001.tb10601.x
Haebel S, Bahrke S, Peter MG (2007) Quantitative sequencing of complex mixtures of heterochitooligosaccharides by MALDI-linear ion trap mass spectrometry. Anal Chem 79(15):5557–5566. https://doi.org/10.1021/ac062254u
Harwood JL (1998) Plant lipid biosynthesis: fundamentals and agricultural applications. Cambridge Unviersity Press, New York
Hua Y, Zhang M, Fu C, Chen Z, Chan GYS (2004) Structural characterization of a 2-O-acetylglucomannan from Dendrobium officinale stem. Carbohydr Res 339:2219–2224. https://doi.org/10.1016/j.carres.2004.05.034
Kačuráková M, Wilson RH (2001) Developments in mid-infrared FT-IR spectroscopy of selected carbohydrates. Carbohydr Polym 44:291–303. https://doi.org/10.1016/S0144-8617(00)00245-9
Kananont N, Pichyangkura R, Chanprame S, Chadchawan S, Limpanavech P (2010) Chitosan specificity for the in vitro seed germination of two Dendrobium orchids (Asparagales: Orchidaceae). Sci Hortic 124:239–247. https://doi.org/10.1016/j.scienta.2009.11.019
Kıran Acemi R, Acemi A (2019) Polymerization degree-dependent changes in the effects of in vitro chitosan treatments on photosynthetic pigment, protein, and dry matter contents of Ipomoea purpurea. EuroBiotech J 3(4):197–202. https://doi.org/10.2478/ebtj-2019-0024
Knudson L (1946) A new nutrient solution for germination of orchid seed. Amer Orchid Soc Bull 15:214–217
Kowalski B, Terry FJ, Herrera L, Peñalver DA (2006) Application of soluble chitosan in vitro and in the greenhouse to increase yield and seed quality of potato minitubers. Potato Res 49:167–176. https://doi.org/10.1007/s11540-006-9015-0
Lahlali R, Jiang Y, Kumar S, Karunakaran C, Liu X, Borondics F, Hallin E, Bueckert R (2014) ATR-FT-IR spectroscopy reveals involvement of lipids and proteins of intact pea pollen grains to heat stress tolerance. Front Plant Sci 5:747. https://doi.org/10.3389/fpls.2014.00747
Laurent N, Der C, Simon-Plas F, Gerbeau-Pissot P (2019) Cell stage appears critical for control of plasma membrane order in plant cells. Plant Signal Behav 14(8):e1620058. https://doi.org/10.1080/15592324.2019.1620058
Luan LQ, Ha VTT, Nagasawa N, Kume T, Yoshii F, Nakanishi TM (2005) Biological effect of irradiated chitosan on plants in vitro. Biotechnol Appl Biochem 41(1):49–57. https://doi.org/10.1042/BA20030219
Manohar N, Jayaramudu J, Suchismita S, Rajkumar K, Babul Reddy A, Sadiku ER, Priti R, Maurya DJ (2017) A unique application of the second order derivative of FT-IR–ATR spectra for compositional analyses of natural rubber and polychloroprene rubber and their blends. Polym Test 62:447–453. https://doi.org/10.1016/j.polymertesting.2017.07.030
Mondal MMA, Malek MA, Puteh AB, Ismail MR, Ashrafuzzaman M, Naher L (2012) Effect of foliar application of chitosan on growth and yield in okra. Aust J Crop Sci 6(5):918–921
Monnier G, Frahm E, Luo B, Missal K (2017) Develo** FT-IR microspectroscopy for analysis of plant residues on stone tools. J Archaeol Sci 78:158–178. https://doi.org/10.1016/j.jas.2016.12.004
Movasaghi Z, Rehman S, Rehman I (2008) Fourier transform infrared (FT-IR) spectroscopy of biological tissues. Appl Spectrosc Rev 43:134–179. https://doi.org/10.1080/05704920701829043
Nge KL, New N, Chandrkrachang S, Stevens WF (2006) Chitosan as a growth stimulator in orchid tissue culture. Plant Sci 170:1185–1190. https://doi.org/10.1016/j.plantsci.2006.02.006
Owen AJ (1995) Uses of derivative spectroscopy—application note, agilent technologies. https://www.whoi.edu/cms/files/derivative_spectroscopy_59633940_175744.pdf. Accessed 03 Sept 2019
Ozek NS, Bal IB, Sara Y, Onur R (1840) Severcan F (2014) Structural and functional characterization of simvastatin-induced myotoxicity in different skeletal muscles. Biochim Biophys Acta 1:406–415. https://doi.org/10.1016/j.bbagen.2013.09.010
Palacio S, Aitkenhead M, Escudero A, Montserrat-Martí G, Maestro M, Robertson AHJ (2014) Gypsophile chemistry unveiled: Fourier transform infrared (FT-IR) spectroscopy provides new insight into plant adaptations to gypsum soils. PLoS ONE 9(9):e107285. https://doi.org/10.1371/journal.pone.0107285
Pornpienpakdee P, Singhasurasak R, Chaiyasap P, Pichyangkura R, Bunjongrat R, Chadchawan S, Limpanavech P (2010) Improving the micropropagation efficiency of hybrid Dendrobium orchids with chitosan. Sci Hortic 124(4):490–499. https://doi.org/10.1016/j.scienta.2010.02.008
Rademacher W (2015) Plant growth regulators: backgrounds and uses in plant production. J Plant Growth Regul 34:845–872. https://doi.org/10.1007/s00344-015-9541-6
Ramos-García M, Ortega-Centeno S, Hernández-Lauzardo AN, Alia-Tejacal I, Bosquez-Molina E, Bautista-Baños S (2009) Response of gladiolus (Gladiolus spp) plants after exposure corms to chitosan and hot water treatments. Sci Hortic 121(4):480–484. https://doi.org/10.1016/j.scienta.2009.03.002
Salvador VH, Lima RB, dos Santos WD, Soares AR, Böhm PAF, Marchiosi R, Ferrarese MRR, Ferrarese-Filho O (2013) Cinnamic acid increases lignin production and inhibits soybean root growth. PLoS ONE 8(7):e69105. https://doi.org/10.1371/journal.pone.0069105
Sarabia LD, Boughton BA, Rupasinghe T, van de Meene AML, Callahan DL, Hill CB, Roessner U (2018) High-mass-resolution MALDI mass spectrometry imaging reveals detailed spatial distribution of metabolites and lipids in roots of barley seedlings in response to salinity stress. Metabolomics 14(5):63. https://doi.org/10.1007/s11306-018-1359-3
Schatz C, Viton C, Delair T, Pichot C, Domard A (2003) Typical physicochemical behaviors of chitosan in aqueous solution. Biomacromol 4:641–648. https://doi.org/10.1021/bm025724c
Shih M, Hsieh T, Lin T, Hsing YC, Hoekstra FA (2010) Characterization of two soybean (Glycine max L) LEA IV proteins by circular dichroism and Fourier transform infrared spectrometry. Plant Cell Physiol 51(3):395–407. https://doi.org/10.1093/pcp/pcq005
Suresh S, Karthikeyan S, Jayamoorthy K (2016) FT-IR and multivariate analysis to study the effect of bulk and nano copper oxide on peanut plant leaves. J Sci 1(3):343–357. https://doi.org/10.1016/j.jsamd.2016.08.004
Szymanska-Chargot M, Zdunek A (2013) Use of FT-IR spectra and PCA to the bulk characterization of cell wall residues of fruits and vegetables along a fraction process. Food Biophys 8(1):29–42. https://doi.org/10.1007/s11483-012-9279-7
Türker S, Dogan M, Severcan F (2007) The characterization and differentiation of higher plants by Fourier transform infrared spectroscopy. Appl Spectrosc 61:300–308. https://doi.org/10.1366/000370207780220903
Türker-Kaya S, Huck CW (2017) A Review of mid-infrared and near-infrared imaging: principles, concepts and applications in plant tissue analysis. Molecules 22(1):168. https://doi.org/10.3390/molecules22010168
Türker-Kaya S, Mutlu O, Celikyurt I, Akar F, Ulak G (2016) Tianeptine, Olanzapine and Fluoxetine show similar restoring effects on stress induced molecular changes in mice brain: an FT-IR study. Spectrochim Acta A 161:178–185. https://doi.org/10.1016/j.saa.2016.02.038
Vårum KM, Anthonsen MW, Grasdalen H, Smidsrød O (1991) Determination of degree of N-acetylation and the distribution of N-acetyl groups in partially N-deacetylated chitins (chitosans) by high field NMR spectroscopy. Carbohydr Res 211(1):17–23. https://doi.org/10.1016/0008-6215(91)84142-2
Wang Y (2012) Application of Fourier transform infrared microspectroscopy (FT-IR) and thermogravimetric analysis (TGA) for quick identification of Chinese herb Solanum lyratum. Plant Omics 5(6):508–513
White KE, Reeves JB, Coale FJ (2016) Cell wall compositional changes during incubation of plant roots measured by mid-infrared diffuse reflectance spectroscopy and fiber analysis. Geoderma 264:205–213. https://doi.org/10.1016/j.geoderma.2015.10.018
Wilson RH, Smith AC, Kačuráková M, Saunders PK, Wellner N, Waldron KW (2000) The mechanical properties and molecular dynamics of plant cell wall polysaccharides studied by Fourier-transform infrared spectroscopy. Plant Physiol 124:397–405. https://doi.org/10.1104/pp.124.1.397
Zhang H, Yamamoto Y, Ishikawa Y, Carpentier R (1999) Characterization of the secondary structure and thermostability of the extrinsic 16 kilodalton protein of spinach photosystem II by Fourier transform infrared spectroscopy. J Mol Struct 513:127–132. https://doi.org/10.1016/S0022-2860(99)00107-6
Zhang K, Bhuiya M-W, Pazo JR, Miao Y, Kim H, Ralph J, Liu C-J (2012) An engineered monolignol 4-O-methyltransferase depresses lignin biosynthesis and confers novel metabolic capability in Arabidopsis. Plant Cell 24:3135–3152. https://doi.org/10.1105/tpc.112.101287
Zhou G, Taylor G, Polle A (2011) FTIR-ATR-based prediction and modelling of lignin and energy contents reveals independent intra-specific variation of these traits in bioenergy poplar. Plant Methods 7:12–19. https://doi.org/10.1186/1746-4811-7-9
Acknowledgements
The chitosan samples were supplied by Nour Eddine El Gueddari of the University of Münster, Münster, Germany. Nour Eddine El Gueddari passed away on February 8, 2018.
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AA designed and performed the experiments and analyzed the data. AA and STK wrote the manuscript. All authors read and approved the final manuscript.
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Acemi, A., Türker-Kaya, S. Biomolecular Structure and Composition Changes in the Root System of Long-Lipped Serapias (Serapias vomeracea) After In Vitro Chitosan and Plant Growth Regulator Treatments. J Plant Growth Regul 40, 1315–1326 (2021). https://doi.org/10.1007/s00344-020-10191-4
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DOI: https://doi.org/10.1007/s00344-020-10191-4