Evaluation of the Potential of Araucaria angustifolia Seeds as Source of Oligosaccharides, Resistant Starch and Growth of Probiotic Bacteria — Oak Academic Publishing
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Evaluation of the Potential of Araucaria angustifolia Seeds as Source of Oligosaccharides, Resistant Starch and Growth of Probiotic Bacteria
Embrapa Forestry, Colombo, Brazil
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Department of Food Technology, Federal University of Viçosa (UFV), Viçosa, Brazil
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School of Chemical Engineering, The University of Queensland (UQ), Brisbane, Australia
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Department of Food Technology, Center for Technology and Regional Development, Federal University of Paraiba, João Pessoa, Brazil
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Postgraduation Program in Food Science and Technology, Department of Food Engineering, Technology Center, Federal University of Paraiba, João Pessoa, Brazil
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Tropical Roots and Starches Center, Paulista State University (UNESP), Botucatu, Brazil
1 Embrapa Forestry, Colombo, Brazil
2 Department of Food Technology, Federal University of Viçosa (UFV), Viçosa, Brazil
3 School of Chemical Engineering, The University of Queensland (UQ), Brisbane, Australia
4 Department of Food Technology, Center for Technology and Regional Development, Federal University of Paraiba, João Pessoa, Brazil
5 Postgraduation Program in Food Science and Technology, Department of Food Engineering, Technology Center, Federal University of Paraiba, João Pessoa, Brazil
6 Tropical Roots and Starches Center, Paulista State University (UNESP), Botucatu, Brazil
“Pinhão”, the seed of Araucaria angustifolia , is an important food, being part of the eating habits of Indigenous communities. In this study, we evaluated the oligosaccharide content, resistant starch and the growth of probiotic bacteria. GF4 (1-fructofuranosylnystose) was the main fructo-oligosaccharides found, in higher contents compared to other food sources. Maltooligosaccharides (MOS) represented the main part of the oligosaccharides profile of Brazilian pine seeds. In descending order of importance was maltoheptaose (G7), maltohexose (G6) and maltotriose (G3). The starches from the variety Sanct josephi presented the highest amount of resistant starch that could stimulate probiotic strains, mainly B. breve and L. plantarum , and may have a prebiotic effect, potentially promoting health benefits. This study advances the understanding of the chemical composition of the main portion of the “pinhão” enhancing awareness of its potential as a healthy food source, contributing to different uses and indirectly with the species preservation.
KeywordsMaltooligosaccharidesFructooligosaccharidesResistant StarchB. breveL. plantarum
Godoy, R.C.B.d., Deliza, R., Negre, M.D.F.d.O. and Santos, G.G.d. (2018) Consumidor de pinhão: Hábitos, atributos de importância e percepção. Pesquisa Florestal Brasileira , 38, 1-18. https://doi.org/10.4336/2018.pfb.38e201801655
Sampaio, D.A., Garcia, R.A. and Lima, H.R.P. (2019) Anatomical and Physicochemical Characterization of the Araucaria angustifolia Seed Coat. Floresta e Ambiente , 26, e20170867. https://doi.org/10.1590/2179-8087.086717
Carvalho, P.E.R. (1994) Espécies florestais brasileiras: Recomendações silviculturais, potencialidades e uso da madeira. Embrapa.
Cordenunsi, B.R., Wenzel de Menezes, E., Genovese, M.I., Colli, C., Gonçalves de Souza, A. and Lajolo, F.M. (2004) Chemical Composition and Glycemic Index of Brazilian Pine ( Araucaria angustifolia ) Seeds. Journal of Agricultural and Food Chemistry , 52, 3412-3416. https://doi.org/10.1021/jf034814l
Oliveira, V.B., Yamada, L.T., Fagg, C.W. and Brandão, M.G.L. (2012) Native Foods from Brazilian Biodiversity as a Source of Bioactive Compounds. Food Research International , 48, 170-179. https://doi.org/10.1016/j.foodres.2012.03.011
Cunha, I.P.d., Melo, D.W.d., Verruck, S., Maran, B.M., Prudencio, E.S. and Amante, E.R. (2018) Bioaccessibility of Phenolic Compounds of Araucaria angustifolia from Seed Water Extracts during in Vitro Simulated Gastrointestinal Conditions. Food and Nutrition Sciences , 9, 1137-1146. https://doi.org/10.4236/fns.2018.910082
Boff Zortéa-Guidolin, M.E., Piler de Carvalho, C.W., Bueno de Godoy, R.C., Mottin Demiate, I. and Paula Scheer, A. (2017) Influence of Extrusion Cooking on in Vitro Digestibility, Physical and Sensory Properties of Brazilian Pine Seeds Flour ( Araucaria angustifolia ). Journal of Food Science , 82, 977-984. https://doi.org/10.1111/1750-3841.13686
Pigozzi, L., Sganzerla, W.G., Veeck, A.P.D.L. and Conto, L.C. (2019) Evaluation of Cooking Methods in the Phenolic Content and Antioxidant Activity in Araucaria angustifolia Seeds. Chemical Engineering Transactions , 75, 145-150. https://doi.org/10.3303/CET1975025
Al-Sheraji, S.H., Ismail, A., Manap, M.Y., Mustafa, S., Yusof, R.M. and Hassan, F.A. (2013) Prebiotics as Functional Foods: A Review. Journal of Functional Foods , 5, 1542-1553. https://doi.org/10.1016/j.jff.2013.08.009
Sousa, V.M.C.d., Santos, E.F.d. and Sgarbieri, V.C. (2011) The Importance of Prebiotics in Functional Foods and Clinical Practice. Food and Nutrition Sciences , 2, 133-144. https://doi.org/10.4236/fns.2011.22019
Lu, E., Yeung, M. and Yeung, C.K. (2018) Comparative Analysis of Lactulose and Fructooligosaccharide on Growth Kinetics, Fermentation, and Antioxidant Activity of Common Probiotics. Food and Nutrition Sciences , 9, 161-178. https://doi.org/10.4236/fns.2018.93013
Ibrahim, O. (2018) Functional Oligosaccharide: Chemicals Structure, Manufacturing, Health Benefits, Applications and Regulations. Journal of Food Chemistry & Nanotechnology , 4, 65-76. https://doi.org/10.17756/jfcn.2018-060
Chaves, P.F.P., Iacomini, M. and Cordeiro, L.M.C. (2019) Chemical Characterization of Fructooligosaccharides, Inulin and Structurally Diverse Polysaccharides from Chamomile Tea. Carbohydrate Polymers , 214, 269-275. https://doi.org/10.1016/j.carbpol.2019.03.050
Jovanovic-Malinovska, R., Kuzmanova, S. and Winkelhausen, E. (2014) Oligosaccharide Profile in Fruits and Vegetables as Sources of Prebiotics and Functional Foods. International Journal of Food Properties , 17, 949-965. https://doi.org/10.1080/10942912.2012.680221
Belorkar, S.A. and Gupta, A.K. (2016) Oligosaccharides: A Boon from Nature’s Desk. AMB Express , 6, Article No. 82. https://doi.org/10.1186/s13568-016-0253-5
Caetano, B., De Moura, N., Almeida, A., Dias, M., Sivieri, K. and Barbisan, L. (2016) Yacon ( Smallanthus sonchifolius ) as a Food Supplement: Health-Promoting Benefits of Fructooligosaccharides. Nutrients , 8, Article No. 436. https://doi.org/10.3390/nu8070436
He, Z., Zeng, J., Hu, J., Chen, J., Peng, D., Du, B., et al. (2024) Effects of Cooking Methods on the Physical Properties and in Vitro Digestibility of Starch Isolated from Chinese Yam. International Journal of Biological Macromolecules , 267, Article ID: 131597. https://doi.org/10.1016/j.ijbiomac.2024.131597
Patel, S. and Goyal, A. (2010) Functional Oligosaccharides: Production, Properties and Applications. World Journal of Microbiology and Biotechnology , 27, 1119-1128. https://doi.org/10.1007/s11274-010-0558-5
Raigond, P., Ezekiel, R. and Raigond, B. (2014) Resistant Starch in Food: A Review. Journal of the Science of Food and Agriculture , 95, 1968-1978. https://doi.org/10.1002/jsfa.6966
Bede, D. and Zaixiang, L. (2020) Recent Developments in Resistant Starch as a Functional Food. Starch - Stärke , 73, 3-4. https://doi.org/10.1002/star.202000139
Birt, D.F., Boylston, T., Hendrich, S., Jane, J., Hollis, J., Li, L., et al. (2013) Resistant Starch: Promise for Improving Human Health. Advances in Nutrition , 4, 587-601. https://doi.org/10.3945/an.113.004325
Reed, M.O., Ai, Y., Leutcher, J.L. and Jane, J. (2013) Effects of Cooking Methods and Starch Structures on Starch Hydrolysis Rates of Rice. Journal of Food Science , 78, H1076-H1081. https://doi.org/10.1111/1750-3841.12165
Piatti, C., Graeff-Hönninger, S. and Khajehei, F. (2019) The Demand for Superfoods: Consumers’ Desire, Production Viability and Bio-Intelligent Transition. In: Piatti, C., Graeff-Hönninger, S. and Khajehei, F., Eds., Food Tech Trans : Reconnecting Agri-food , Technology and Society , Springer, 81-94. https://doi.org/10.1007/978-3-030-21059-5
Scott, K.P., Grimaldi, R., Cunningham, M., Sarbini, S.R., Wijeyesekera, A., Tang, M.L.K., et al. (2019) Developments in Understanding and Applying Prebiotics in Research and Practice—An ISAPP Conference Paper. Journal of Applied Microbiology , 128, 934-949. https://doi.org/10.1111/jam.14424
Araldi, C.G., Coelho, C.M.M. and Shibata, M. (2018) Storage Potential of Local Brazilian Pine Seed Varieties. Floresta e Ambiente , 25, e.00016815. https://doi.org/10.1590/2179-8087.016815
Shibata, M., Coelho, C.M.M., de Garighan, J.A., dos Santos, H.P., Araldi, C.G. and Maraschin, M. (2021) Seed Development of Araucaria angustifolia : Plant Hormones and Germinability in 2 Years of Seeds Production. New Forests , 52, 759-775. https://doi.org/10.1007/s11056-020-09821-2
Pereira, G.A., Arruda, H.S., Molina, G. and Pastore, G.M. (2017) Extraction Optimization and Profile Analysis of Oligosaccharides in Banana Pulp and Peel. Journal of Food Processing and Preservation , 42, e13408. https://doi.org/10.1111/jfpp.13408
L’homme, C., Peschet, J.L., Puigserver, A. and Biagini, A. (2001) Evaluation of Fructans in Various Fresh and Stewed Fruits by High-Performance Anion-Exchange Chromatography with Pulsed Amperometric Detection. Journal of Chromatography A , 920, 291-297. https://doi.org/10.1016/s0021-9673(00)01262-0
Goñi, I., García-Diz, L., Mañas, E. and Saura-Calixto, F. (1996) Analysis of Resistant Starch: A Method for Foods and Food Products. Food Chemistry , 56, 445-449. https://doi.org/10.1016/0308-8146(95)00222-7
Costa, F.J.O.G., Couto, J.M., Waszczynskyj, N., Godoy, R.C.B., Carvalho, C.W.P. and Walter, E.H.M. (2014) Extração de amido de pinhão. Embrapa Florestas, Comunicado Técnico 349.
Yıldız, S. (2010) The Metabolism of Fructooligosaccharides and Fructooligosaccharide-Related Compounds in Plants. Food Reviews International , 27, 16-50. https://doi.org/10.1080/87559129.2010.518295
Mellado-Mojica, E., González de la Vara, L.E. and López, M.G. (2016) Fructan Active Enzymes (FAZY) Activities and Biosynthesis of Fructooligosaccharides in the Vacuoles of Agave tequilana Weber Blue Variety Plants of Different Age. Planta , 245, 265-281. https://doi.org/10.1007/s00425-016-2602-7
Grzelak-Błaszczyk, K., Kołodziejczyk, K., Badełek, E. and Adamicki, F. (2011) Changes in the Contents of Mono-, Di-and Oligosaccharides in Leek Plants Stored in Cold Room. European Food Research and Technology , 232, 1027-1033. https://doi.org/10.1007/s00217-011-1476-y
Sancho, R.A.S., Souza, J.D.R.P., de Lima, F.A. and Pastore, G.M. (2017) Evaluation of Oligosaccharide Profiles in Selected Cooked Tubers and Roots Subjected to in Vitro Digestion. LWT — Food Science and Technology , 76, 270-277. https://doi.org/10.1016/j.lwt.2016.07.046
Jovanovic-Malinovska, R., Kuzmanova, S. and Winkelhausen, E. (2015) Application of Ultrasound for Enhanced Extraction of Prebiotic Oligosaccharides from Selected Fruits and Vegetables. Ultrasonics Sonochemistry , 22, 446-453. https://doi.org/10.1016/j.ultsonch.2014.07.016
Isejima, E.M. and Figueiredo-Ribeiro, R.d.C.L. (1993) Fructan Variations in Tuberous Roots of Viguiera Discolor Baker (Asteraceae): The Influence of Phenology. Plant and Cell Physiology , 34, 723-727. https://doi.org/10.1093/oxfordjournals.pcp.a078475
Li, W., Zhang, J., Yu, C., Li, Q., Dong, F., Wang, G., et al. (2015) Extraction, Degree of Polymerization Determination and Prebiotic Effect Evaluation of Inulin from Jerusalem Artichoke. Carbohydrate Polymers , 121, 315-319. https://doi.org/10.1016/j.carbpol.2014.12.055
Sridevi, V., Sumathi, V., Prasad, M.G. and Satish, K.M. (2014) Fructooligosaccharides—Type Prebiotic: A Review. Journal of Pharmacy Research , 8, 321-330.
Bláhová, M., Štefuca, V., Hronská, H. and Rosenberg, M. (2023) Maltooligosaccharides: Properties, Production and Applications. Molecules , 28, Article No. 3281. https://doi.org/10.3390/molecules28073281
Brito, T.B.N., Pereira, A.P.A., Pastore, G.M., Moreira, R.F.A., Ferreira, M.S.L. and Fai, A.E.C. (2020) Chemical Composition and Physicochemical Characterization for Cabbage and Pineapple By-Products Flour Valorization. LWT , 124, Article ID: 109028. https://doi.org/10.1016/j.lwt.2020.109028
Joyet, P., Mokhtari, A., Riboulet-Bisson, E., Blancato, V.S., Espariz, M., Magni, C., et al. (2017) Enzymes Required for Maltodextrin Catabolism in Enterococcus faecalis Exhibit Novel Activities. Applied and Environmental Microbiology , 83, 1-15. https://doi.org/10.1128/aem.00038-17
Hampp, R., Mertz, A., Schaible, R., Schwaigerer, M. and Nehls, U. (2000) Distinction of Araucaria angustifolia Seeds from Different Locations in Brazil by a Specific DNA Sequence. Trees , 14, 429-434. https://doi.org/10.1007/s004680000060
Gangola, M.P., Jaiswal, S., Khedikar, Y.P. and Chibbar, R.N. (2014) A Reliable and Rapid Method for Soluble Sugars and RFO Analysis in Chickpea Using HPAEC-PAD and Its Comparison with HPLC-RI. Food Chemistry , 154, 127-133. https://doi.org/10.1016/j.foodchem.2013.12.085
Williams, B., Grant, L., Gidley, M. and Mikkelsen, D. (2017) Gut Fermentation of Dietary Fibres: Physico-Chemistry of Plant Cell Walls and Implications for Health. International Journal of Molecular Sciences , 18, Article No. 2203. https://doi.org/10.3390/ijms18102203
Yang, L., Liu, Y., Yang, J., Du, C. and Zhai, L. (2021) Changes in the Multi-Scale Structure and Physicochemical Properties of Starch during Potato Growth. Journal of the Science of Food and Agriculture , 101, 5927-5937. https://doi.org/10.1002/jsfa.11245
Teixeira, N.d.C., Queiroz, V.A.V., Rocha, M.C., Amorim, A.C.P., Soares, T.O., Monteiro, M.A.M., et al. (2016) Resistant Starch Content among Several Sorghum (Sorghum Bicolor) Genotypes and the Effect of Heat Treatment on Resistant Starch Retention in Two Genotypes. Food Chemistry , 197, 291-296. https://doi.org/10.1016/j.foodchem.2015.10.099
Nguyen Minh, T., Beverly Cheruto, T., Kieu Minh, V., Phan Thi Truc, L., Phan Thi Thanh, T., Nguyen Bich, T., et al. (2022) Resistant Starch in Various Starchy Vegetables and the Relationship with Its Physical and Chemical Characteristics. Journal of Applied Biology & Biotechnology , 10, 181-188. https://doi.org/10.7324/jabb.2021.100122
Fei, Y., Chen, Z., Han, S., Zhang, S., Zhang, T., Lu, Y., et al. (2021) Role of Prebiotics in Enhancing the Function of Next-Generation Probiotics in Gut Microbiota. Critical Reviews in Food Science and Nutrition , 63, 1037-1054. https://doi.org/10.1080/10408398.2021.1958744
Echegaray, N., Yilmaz, B., Sharma, H., Kumar, M., Pateiro, M., Ozogul, F., et al. (2023) A Novel Approach to Lactiplantibacillus plantarum : From Probiotic Properties to the Omics Insights. Microbiological Research , 268, Article ID: 127289. https://doi.org/10.1016/j.micres.2022.127289
Liang, T., Xie, X., Wu, L., Li, L., Yang, L., Jiang, T., et al. (2023) Metabolism of Resistant Starch RS3 Administered in Combination with Lactiplantibacillus plantarum Strain 84-3 by Human Gut Microbiota in Simulated Fermentation Experiments in Vitro and in a Rat Model. Food Chemistry , 411, Article ID: 135412. https://doi.org/10.1016/j.foodchem.2023.135412
You, S., Ma, Y., Yan, B., Pei, W., Wu, Q., Ding, C., et al. (2022) The Promotion Mechanism of Prebiotics for Probiotics: A Review. Frontiers in Nutrition , 9, Article ID: 1000517. https://doi.org/10.3389/fnut.2022.1000517