Abstract
Fruit softening during ripening is mainly a consequence of the solubilization and depolymerization of cell wall components mediated by the action of a complex set of enzymes and proteins. In the present work, we performed a comparative study of the changes in physiological properties and cell wall-associated polysaccharide contents during different developmental stages of strawberry fruit (Fragaria × ananassa Duch. cultivar Camarosa) using thermogravimetry (TG) combined with Fourier transform infrared and physiological analyses. The Camarosa cultivar showed a decline in the fruit firmness, based on the TGA curves was demonstrated the degradation of the cell wall polymers. Additionally, the TG analysis showed that the dry sample derived from the green stage fruit had the greatest thermal stability, most likely due to the increase in inter-chain hydrogen bonding within the cell wall, while the sample derived from the ripe stage fruit had the least thermal stability. Finally, the existence of a correlation between fruit firmness and mass loss at specific temperatures, that provides a basis for a model for understanding the changes within the cell wall in F. × ananassa during fruit ripening.
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Avila-Salas F, Rodriguez-Nuñez Y, Marican A, Castro R, Villaseñor J, Santos L, Wehinger S, Durán-Lara E (2018) Rational development of a novel hydrogel as a pH-sensitive controlled release system for nifedipine. Polymers 10:806. https://doi.org/10.3390/polym10070806
Brummell DA (2006) Cell wall disassembly in ripening fruit. Funct Plant Biol 33:103–119
Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–339
Chundawat SPS, Beckham GT, Himmel ME, Dale BE (2011) Deconstruction of lignocellulosic biomass to fuels and chemicals. Annu Rev Chem Biomol Eng 2:121–145
Collard F-X, Blin J (2014) A review on pyrolysis of biomass constituents: mechanisms and composition of the products obtained from the conversion of cellulose, hemicelluloses and lignin. Renew Sust Energy Rev 38:594–608
Concha CM, Figueroa NE, Poblete LA, Oñate FA, Schwab W, Figueroa CR (2013) Methyl jasmonate treatment induces changes in fruit ripening by modifying the expression of several ripening genes in Fragaria chiloensis fruit. Plant Physiol Biochem 70:433–444
Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol Biochem 38:109–124
Dotto MC, Martínez GA, Civello PM (2006) Expression of expansin genes in strawberry varieties with contrasting fruit firmness. Plant Physiol Biochem 44:301–307
Estrada B, Bernal MA, Díaz J, Pomar F, Merino F (2000) Fruit development in Capsicum annuum: changes in capsaicin, lignin, free phenolics, and peroxidase patterns. J Agric Food Chem 48:6234–6239
Fengel D (1993) Influence of water on the OH valency range in deconvoluted FTIR spectra of cellulose. Holzforschung 47:103–108
Fengel D, Ludwig M (1991) Möglichkeiten und grenzen der FTIR-spektroskopie bei der charakterisierung von cellulose. I: vergleich von verschiedenen cellulosefasern und bakterien-cellulose. Das Pap 45:45–51
Figueroa CR, Pimentel P, Gaete-Eastman C, Moya M, Herrera R, Caligari PDS, Moya-León MA (2008) Softening rate of the Chilean strawberry (Fragaria chiloensis) fruit reflects the expression of polygalacturonase and pectate lyase genes. Postharvest Biol Technol 49:210–220
Figueroa CR, Rosli HG, Civello PM, Martínez GA, Herrera R, Moya-León MA (2010) Changes in cell wall polysaccharides and cell wall degrading enzymes during ripening of Fragaria chiloensis and Fragaria× ananassa fruits. Sci Hortic 124:454–462
Forero-Doria O, Castro R, Gutiérrez M, González-Valenzuela D, Santos L, Ramirez D, Guzman L (2018) Novel alkylimidazolium ionic liquids as an antibacterial alternative to pathogens of the skin and soft tissue infections. Molecules 23:2354. https://doi.org/10.3390/molecules23092354
Fraeye I, De Roeck A, Duvetter T, Verlent I, Hendrickx M, Van Loey A (2007) Influence of pectin properties and processing conditions on thermal pectin degradation. Food Chem 105:555–563
Ghaffari A, Navaee K, Oskoui M, Bayati K, Rafiee-Tehrani M (2007) Preparation and characterization of free mixed-film of pectin/chitosan/Eudragit® RS intended for sigmoidal drug delivery. Eur J Pharm Biopharm 67:175–186
Harris PJ, Stone BA (2008) Chemistry and molecular organization of plant cell walls. In: Himmel ME (ed) Biomass recalcitrance: deconstructing the plant cell wall for bioenergy. Blackwell, Oxford, pp 61–93
Huber DJ (1984) Strawberry fruit softening: the potential roles of polyuronides and hemicelluloses. J Food Sci 49:1310–1315
Indran S, Raj RE, Sreenivasan VS (2014) Characterization of new natural cellulosic fiber from Cissus quadrangularis root. Carbohyd Polym 110:423–429
Johansson P, Brumer H, Baumann MJ, Kallas ÅM, Henriksson H, Denman SE, Teeri TT, Jones TA (2004) Crystal structures of a poplar xyloglucan endotransglycosylase reveal details of transglycosylation acceptor binding. Plant Cell 16:874–886
Kacurakova M, Capek P, Sasinkova V, Wellner N, Ebringerova A (2000) FT-IR study of plant cell wall model compounds: pectic polysaccharides and hemicelluloses. Carbohyd Polym 43:195–203
Knee M, Sargent JA, Osborne DJ (1977) Cell wall metabolism in developing strawberry fruits. J Exp Bot 28:377–396
Li Q, Liao G, Tian J, Xu Z (2018a) Preparation of novel fluorinated copolyimide/amine-functionalized sepia eumelanin nanocomposites with enhanced mechanical, thermal, and UV-shielding properties. Macromol Mater Eng 303:1700407
Li Q, Li J, Liao G, Xu Z (2018b) The preparation of heparin-like hyperbranched polyimides and their antithrombogenic, antibacterial applications. J Mater Sci Mater Med 29:126. https://doi.org/10.1007/s10856-018-6137-2
Liao G, Chen J, Zeng W, Yu C, Yi C, Xu Z (2016) Facile preparation of uniform nanocomposite spheres with loading silver nanoparticles on polystyrene-methyl acrylic acid spheres for catalytic reduction of 4-nitrophenol. J Phys Chem C 120:25935–25944
Liao G, Li Q, Zhao W, Pang Q, Gao H, Xu Z (2018) In-situ construction of novel silver nanoparticle decorated polymeric spheres as highly active and stable catalysts for reduction of methylene blue dye. Appl Catal A 549:102–111
Liu C, Wyman CE (2005) Partial flow of compressed-hot water through corn stover to enhance hemicellulose sugar recovery and enzymatic digestibility of cellulose. Bioresour Technol 96:1978–1985
Lu Q, X-c Yang, C-q Dong, Z-f Zhang, X-m Zhang, X-f Zhu (2011) Influence of pyrolysis temperature and time on the cellulose fast pyrolysis products: analytical Py-GC/MS study. J Anal Appl Pyrol 92:430–438
Mamleev V, Bourbigot S, Le Bras M, Yvon J (2009) The facts and hypotheses relating to the phenomenological model of cellulose pyrolysis: interdependence of the steps. J Anal Appl Pyrol 84:1–17
Manning K (1993) Soft fruit. In: Seymour GB, Taylor JE, Tucker GA (eds) Biochemistry of fruit ripening. Chapman and Hall, London, pp 347–377
Marchessault RH, Sundararajan PR (1983) Cellulose. In: Aspinall GO (ed) The polysaccharides, vol 2. Academic Press Inc., New York, pp 11–95
Marga F, Grandbois M, Cosgrove DJ, Baskin TI (2005) Cell wall extension results in the coordinate separation of parallel microfibrils: evidence from scanning electron microscopy and atomic force microscopy. Plant J 43:181–190
McGrath TE, Chan WG, Hajaligol MR (2003) Low temperature mechanism for the formation of polycyclic aromatic hydrocarbons from the pyrolysis of cellulose. J Anal Appl Pyrol 66:51–70
Minic Z (2008) Physiological roles of plant glycoside hydrolases. Planta 227:723
Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin in Plant Biol 11:266–277
Morán JI, Alvarez VA, Cyras VP, Vázquez A (2008) Extraction of cellulose and preparation of nanocellulose from sisal fibers. Cellulose 15:149–159
Nardi C, Escudero C, Villarreal N, Martínez G, Civello PM (2013) The carbohydrate-binding module of Fragaria× ananassa expansin 2 (CBM-FaExp2) binds to cell wall polysaccharides and decreases cell wall enzyme activities “in vitro”. J Plant Res 126:151–159
Nardi CF, Villarreal NM, Rossi FR, Martínez S, Martínez GA, Civello PM (2015) Overexpression of the carbohydrate binding module of strawberry expansin2 in Arabidopsis thaliana modifies plant growth and cell wall metabolism. Plant Mol Biol 88:101–117
O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139
Pandey KK (1999) A study of chemical structure of soft and hardwood and wood polymers by FTIR spectroscopy. J Appl Polym Sci 71:1969–1975
Pandey KK, Pitman AJ (2003) FTIR studies of the changes in wood chemistry following decay by brown-rot and white-rot fungi. Int Biodeterior Biodegrad 52:151–160
Payasi A, Mishra NN, Chaves ALS, Singh R (2009) Biochemistry of fruit softening: an overview. Physiol Mol Biol Plants 15:103–113
Perkins-Veazie P (1995) Growth and ripening of strawberry fruit. Hortic Rev 17:267–297
Pilling E, Höfte H (2003) Feedback from the wall. Curr Opin Plant Biol 6:611–616
Poletto M, Zattera AJ, Santana RMC (2012) Structural differences between wood species: evidence from chemical composition, FTIR spectroscopy, and thermogravimetric analysis. J Appl Polym Sci 126:E337–E344
Posé S, García-Gago JA, Santiago-Doménech N, Pliego-Alfaro F, Quesada MA, Mercado JA (2011) Strawberry fruit softening: role of cell wall disassembly and its manipulation in transgenic plants. Genes Genomes Genomics 5:40–48
Purves CB (1954) Chain structure. In: Ott E, Spurlin HM, Grafflin MW (eds) Cellulose and cellulose derivatives. Part I. Wiley-Interscience, New York, pp 54–98
Ramos P, Parra-Palma C, Figueroa CR, Zuñiga PE, Valenzuela-Riffo F, Gonzalez J, Gaete-Eastman C, Morales-Quintana L (2018) Cell wall-related enzymatic activities and transcriptional profiles in four strawberry (Fragaria × ananassa) cultivars during fruit development and ripening. Sci Hortic 238:325–332
Redgwell RJ, Fischer M, Kendal E, MacRae EA (1997) Galactose loss and fruit ripening: high-molecular-weight arabinogalactans in the pectic polysaccharides of fruit cell walls. Planta 203:174–181
Redondo-Nevado J, Moyano E, Medina-Escobar N, Caballero JL, Muñoz-Blanco J (2001) A fruit-specific and developmentally regulated endopolygalacturonase gene from strawberry (Fragaria × ananassa cv. Chandler). J Exp Bot 52:1941–1945
Ring L, Yeh S-Y, Hücherig S, Hoffmann T, Blanco-Portales R, Fouche M, Villatoro C, Denoyes B, Monfort A, Caballero JL, Muñoz-Blanco J, Gershenson J, Schwab W (2013) Metabolic interaction between anthocyanin and lignin biosynthesis is associated with peroxidase FaPRX27 in strawberry fruit. Plant Physiol 163:43–60
Rosa MF, Medeiros ES, Malmonge JA, Gregorski KS, Wood DF, Mattoso LHC, Glenn G, Orts WJ, Imam SH (2010) Cellulose nanowhiskers from coconut husk fibers: effect of preparation conditions on their thermal and morphological behavior. Carbohyd Polym 81:83–92
Rose JKC, Bennett AB (1999) Cooperative disassembly of the cellulose–xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci 4:176–183
Rosli HG, Civello PM, Martinez GA (2004) Changes in cell wall composition of three Fragaria × ananassa cultivars with different softening rate during ripening. Plant Physiol Biochem 42:823–831
Sain M, Panthapulakkal S (2006) Bioprocess preparation of wheat straw fibers and their characterization. Ind Crop Prod 23:1–8
Schwanninger M, Rodrigues JC, Pereira H, Hinterstoisser B (2004) Effects of short-time vibratory ball milling on the shape of FT-IR spectra of wood and cellulose. Vib Spectrosc 36:23–40
Shen DK, Gu S, Luo KH, Wang SR, Fang MX (2010) The pyrolytic degradation of wood-derived lignin from pulping process. Bioresour Technol 101:6136–6146
Sun XF, Xu F, Sun RC, Fowler P, Baird MS (2005) Characteristics of degraded cellulose obtained from steam-exploded wheat straw. Carbohyd Res 340:97–106
Vaaje-Kolstad G, Farkaš V, Hrmova M, Fincher GB (2010) Xyloglucan xyloglucosyl transferases from barley (Hordeum vulgare L.) bind oligomeric and polymeric xyloglucan molecules in their acceptor binding sites. Biochim Biophys Acta Gen Subj 1800:674–684
Valenzuela-Riffo F, Ramos P, Morales-Quintana L (2018) Computational study of FaEXPA1 a strawberry alpha expansin protein, through molecular modeling and molecular dynamics simulation studies. Comput Biol Chem 76:79–86
Van de Velden M, Baeyens J, Brems A, Janssens B, Dewil R (2010) Fundamentals, kinetics and endothermicity of the biomass pyrolysis reaction. Renewable Energy 35:232–242
Vicente AR, Saladie M, Rose JKC, Labavitch JM (2007) The linkage between cell wall metabolism and fruit softening: looking to the future. J Sci Food Agric 87:1435–1448
Villarreal NM, Rosli HG, Martínez GA, Civello PM (2008) Polygalacturonase activity and expression of related genes during ripening of strawberry cultivars with contrasting fruit firmness. Postharvest Biol Technol 47:141–150
Wang S, Wang K, Liu Q, Gu Y, Luo Z, Cen K, Fransson T (2009) Comparison of the pyrolysis behavior of lignins from different tree species. Biotechnol Adv 27:562–567
Xiao B, Sun X, Sun R (2001) Chemical, structural, and thermal characterizations of alkali-soluble lignins and hemicelluloses, and cellulose from maize stems, rye straw, and rice straw. Polym Degrad Stab 74:307–319
Xiao S, Gao R, Lu Y, Li J, Sun Q (2015) Fabrication and characterization of nanofibrillated cellulose and its aerogels from natural pine needles. Carbohyd Polym 119:202–209
Yao H, Tian S (2005) Effects of pre- and post-harvest application of salicylic acid or methyl jasmonate on inducing disease resistance of sweet cherry fruit in storage. Postharvest Biol Technol 35:253–262
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The authors acknowledge the helpful comments and suggestions made by the anonymous reviewers of this manuscript.
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This work was supported by FONDECYT [Grant No. 11150543]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Castro, R.I., Morales-Quintana, L. Study of the cell wall components produced during different ripening stages through thermogravimetric analysis. Cellulose 26, 3009–3020 (2019). https://doi.org/10.1007/s10570-019-02305-3
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DOI: https://doi.org/10.1007/s10570-019-02305-3