Internal transcribed spacer (ITS) sequence-based identification of yeast biota on pomegranate surface and determination of extracellular enzyme profile
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https://orcid.org/0000-0003-0336-3010
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Abstract. Genc TT, Günay M. 2020. Internal transcribed spacer (ITS) sequence-based identification of yeast biota on pomegranate surface and determination of extracellular enzyme profile. Nusantara Bioscience 12: 59-67. Yeasts are the most significant organisms to produce fermented products from different types of fruits such as grape, strawberry and pomegranate. The native yeasts on these fruits contribute to beverages’ quality and aroma during fermentation. Pomegranate is used in fruit juice and wine production because of high antioxidant characteristic. In order to determine yeast microbiota on the pomegranate fruits collected from Gallipoli (Gelibolu), Çanakkale-Turkey, ITS-5.8S rDNA gene region have been utilized. Also, phylogenetic relationships among identified yeast species were assigned by using sequences of ITS-5.8S rDNA gene region. In addition, extracellular enzyme activity of identified yeast strains was detected by using API-ZYM. Kluyveromyces lactis, Aureobasidium pullulans, Hanseniaspora uvarum, Candida zeylanoides, Kwoniella sp., and Metschnikowia pulcherrima and Metschnikowia ziziphicola yeast species were identified on pomegranate surface. Phylogenetic analysis, carried out in ITS-5.8S rDNA gene region of identified yeast strains, revealed the presence of five clades. Kwoniella sp., H. uvarum, M. pulcherrima, and Kl. lactis yeast strains revealed high leucine arylamidase activity. Also valine arylamidase activity was determined in M. pulcherrima and Kl. lactis yeast species. Acid phosphatase activity was determined in H. uvarum and K. lactis yeast species. Uncultured Kwoniella sp. and H. uvarum yeast species displayed high ?-galactosidase and ?-glucosidase activities, respectively.
2019-01-01
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References
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Da?c? KE, D??rak M. 2005. Baz? meyve ekstraktlar?n?n antibakteriyal ve antifungal aktiviteleri. KSÜ Fen ve Mühendislik Dergisi 8 (2): 1-7.
De Curtis E, Torriani, S, Rossi E, De Cicco V. 1996. Selection and use of Metschnikowia Pulcherrima as a biological control agent for postharvest rots of peaches and table grapes. Annali de Microbiologia ed Enzymologia. 46: 45–55.
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Garcia-Martos P, Marin P, Hernandez-Molina JM, Garcia-Agudo L, Aoufi S, Mira J. 2001. Extracellular enzymatic activity in 11 Cryptococcus species. Mycopathologia. 150: 1-4.
Gibson BR, Pham T, Wimalasena T, Box WG, Koivuranta K, Storgards E, Smart KA. 2011. Evaluation of ITS PCR and RFLP for differentiation and identification of brewing yeast and brewery ‘wild’ yeast contaminants. Journal of The Institute of Brewing. 117: 556–568.
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Guillamon JM, Sabate J, Barrio E, Cano J, Querol A. 1998. Rapid identification of wine yeast species based on RFLP analysis of the ribosomal internal transcribed spacer (ITS) region. Archives of Microbiology. 169: 387–392.
Harhangi HR, Steenbakkers PJM, Akhmanova A, Jetten MSM, van der Drift C, Op den Camp HJM. 2002. A highly expressed family 1 ? -glucosidase with transglycosylation capacity from the anaerobic fungus Piromyces sp. E2. Biochimica et Biophysica Acta. 1574: 293–303.
Hierro N, Gonzalez A, Mas A, Guillamon JM. 2004. New PCR-based methods for yeast identification. Journal of Applied Microbiology. 97: 792–801. Doi:10.1111/j.1365-2672.2004.02369.x.
Johnson EA. 2013a. Biotechnology of non-Saccharomyces yeasts—the Ascomycetes Applied Microbiology and Biotechnology 97(2): 503–517. DOI: 10.1007/s00253-012-4497-y
Johnson EA. 2013b. Biotechnology of non-Saccharomyces yeasts—the Basidiomycetes Applied Microbiology and Biotechnology. 97(17): 7563–7577. DOI: 10.1007/s00253-013-5046-z
Karasova P, Spiwok V, Mala S, Kralova B, Russell NJ. 2002: Beta-galactosidase activity in psychrotrophic microorganisms and their potential use in food industry. Czech Journal of Food Sciences. 20: 43–47.
Keerti GA, Kumar V, Dubey A, Verma AK. 2014. Kinetic characterization and effect of immobilized thermostable ?-glucosidase in alginate gel Beads on sugarcane juice. ISRN Biochemistry, Article ID 178498, 8 Pages.
K?l?çgün H, Arda N, Uçar EÖ. 2015. Identification of longevity, fertility and growth-promoting properties of pomegranate in Caenorhabditis elegans. Pharmacognosy magazine. 11: 356–359.
Kreger-van Rij NJW. 1984. The yeast, a taxonomic study. Amsterdam, the Netherlands: Elsevier Science B.V.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35: 1547-1549.
Kurtzman CP, Fell JW. 1998. The yeasts: a taxonomic study, 4th edn. Amsterdam: Elsevier Science Publishers.
Kurtzman CP, Robnett CJ. 1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek. 73: 331–371.
Lee BH. 1996. Fundamentals of food biotechnology, VCH Publishers, USA.
Li D, Li X, Dang W, Tran PL, Park S, Oh B, Hong W, Lee J, Park K. 2013. Characterization and application of an acidophilic and thermostable ?-glucosidase from Thermofilum pendens. Journal of Bioscience and Bioengineering. 115(5): 490–496.
Liu HM, Guo JH, Cheng YJ, Luo L, Liu P, Wang BQ, Deng BX, Long CA. 2010a. Improvement of Hanseniaspora uvarum biocontrol activity against gray mold by the addition of ammonium molybdate and the possible mechanisms involved. Crop Protection. 29: 277–282.
Liu HM, Guo JH, Cheng YJ, Luo L, Liu P, Wang BQ, Deng BX, Long CA. 2010b Control of gray mold of grape by Hanseniaspora uvarum and its effects on postharvest quality parameters. Annals of Microbiology. 60: 31–35.
Lopez V, Querol A, Ramon D, Fernandez-Espinar MT. 2001. A simplified procedure to analyze mitochondrial DNA from industrial yeasts. International Journal of Food Microbiology. 68: 75–81.
Naumova ES, Korshunova IV, Jespersen L, Naumov GI. 2003. Molecular genetic identification of Saccharomyces sensu stricto strains for African sorghum beer. FEMS Yeast Research. 3: 177–184.
Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York.
Nikolaou E, Andrighetto C, Lombardi A, Nikolaos T. 2007. Heterogeneity in genetic and phenotypic characteristics of Saccharomyces cerevisiae strains isolated from red and white wine fermentations. Food Control 18: 1458–1465.
Nikolaou E, Soufleros EH, Boulompasi E, Tzanetakis N. 2006. Selection of indigenous Saccharomyces cerevisiae strains according to their oneological characteristics and vinification results. Food Microbiology. 23 (3): 205-211.
Piano S, Neyrotti V, Migheli Q., Gullino ML. 1997. Biocontrol capability of Metschnikowia pulcherrima against Botrytis postharvest rot of apple. Postharvest Biology and Technology. 11: 131–140.
Ramalho MT, Martin MAM, Cardoso MH, Queiroz MJ, Campos AMO. 1999. Biodegradation of azo dyes by the yeast Candida zeylanoides in batch aerated cultures. Chemosphere 38: 2455-2460.
Rodriguez-Vico F, Clemente-Jimenez JM, Mingorance-Cazorla L, Martinez-Rodriguez S, Las Heras-Vazquez FJ. 2003. Molecular characterization and oenological properties of wine yeasts isolated during spontaneous fermentation of six varieties of grape must. Food Microbiology. 21: 149–155.
Romano P, Capece A, Siesto G, Romaniello R. 2009. Restriction analysis of rDNA regions to differentiate non-Saccharomyces wine species in mixed cultures. Journal of Engineering and Technology Research. 1(4): 068-071.
Sabate J, Cano J, Esteve-Zarzoso B, Guillamon JM. 2002. Isolation and identification of yeast associated with Vineyard and winery by RFLP analysis of ribosomal genes and mitochondrial DNA. Microbiological Research. 157: 267–274.
Santos EV Martinez, AO, Munizaga GT, Reyes JE, Won MP. 2012. Effect of high hydrostatic pressure (HHP) processing on physicochemical properties, bioactive compounds and shelf-life of pomegranate juice. Innovative Food Science & Emerging Technologies. 13: 13–22.
Sena RF, Costelli MC, Gibson LH, Coughlin RW. 2006. Enhanced production of pullulan by two strains of A. pullulans with different concentrations of soybean oil in sucrose solution in batch fermentations. Brazilian Journal of Chemical Engineering. 23(4): 507–515.
Sevda SB, Rodrigues L, 2011. The making of pomegranate wine using yeast immobilized on sodium alginate. African Journal of Food Science. 5: 299–304.
Shaima S, Akram A, Halim SA, Tassaduq R, 2017. Sources of ? -galactosidase and its applications in food industry. 3 Biotechnology. 7 (1): 79. DOI 10.1007/s13205-017-0645-5.
Sherman F, Fink GR, Hicks JB. 1986. Methods in yeast genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
Spadaro D, Vola R, Piano S, Gullino ML. 2002. Mechanisms of action and efficacy of four isolates of the yeast Metschnikowia pulcherrima active against postharvest pathogens on apples. Postharvest Biology and Technology. 24: 123–134.
Török T, Rockhold D, King AD. 1993. Use of electrophoretic karyotyping and DNA-DNA hybridization in yeast identification. International Journal of Food Microbiology. 19: 63–80.
Vasiljevic T, Jelen P. 2001. Production of ?-galactosidase for lactose hydrolysis in milk and products using thermophilic lactic acid bacteria. Innovative Food Science & Emerging Technologies. 2: 75-85.
Vaughan Martini A, Martini A. 1987. Taxonomic revision of the yeast genus Kluyveromyces by nuclear deoxyribonucleic acid reassociation. International Journal of Systematic Bacteriology. 37 (4): 380–385.
Versavaud A, Hallet JN. 1995. Pulsed-Field gel electrophoresis combined with rare-cutting endonucleases for strain identification of Candida famata, Kloeckera apiculata and Schizosaccharomyces pombe with chromosome number and size estimation of the two former. Systematic and Applied Microbiology. 18: 303– 309.
Wang X, Li S, Yang X, Yang S, Zhu M. 2012. Technology prospecting on enzymes: application, Marketing and Engineering. 2(3): 1-11.
White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: A Guide to Methods and Applications Academic Press, San Diego, California, USA.
Yasoubi P, Barzegar M, Sahari MA, Azizi MH. 2007. Total phenolic contents and antioxidant activity of pomegranate (Punica granatum L.) peel extracts. Journal of Agricultural Science and Technology. 9: 35-42.
Aslan A, Can M?, Boydak D. 2014. Anti-Oxidant effects of pomegranate juice on Saccharomyces cerevisiae cell growth. African Journal of Traditional, Complementary, and Alternative Medicines. 11: 14-18.
Baffi MA, Bezerra CS, Arévalo-Villena M, Briones-Pérez AI, Gomes E, Da Silva R. 2010. Isolation and molecular identification of wine yeasts from a Brazilian vineyard. Annals of Microbiology. 61: 75–78.
Bakoyianis V, Kanellaki M, Kalliafas A, Koutinas AA. 1992. Low temperature wine making by immobilized cells on mineral kissiris. Journal of Agricultural and Food Chemistry. 40: 1293-1296.
Baleiras Couto MM, Reizinho RG, Duarte FL. 2005. Partial 26S rDNA restriction analysis as a tool to characterize non-Saccharomyces yeasts present during red wine fermentation. International Journal of Food Microbiology. 102: 49–56.
Barnett JA, Payne RW, Yarrow D. 2000. Yeasts: characteristics and identification. Cambridge: Cambridge University Press.
Bernier B, (1958). The production of polysaccharides by fungi active in the decomposition of wood and forest litter. Canadian Journal of Microbiology. 4: 195–204.
Braduardi, P., Porro, D., (2012). Yeast in biotechnology. In: Feldmann H. Ed., Yeast: Molecular and cell biology, Wiley-Blackwell, Germany.
Cadez N, Raspor P, de Cock AW, Boekhout T, Smith MT, 2002. Molecular identification and genetic diversity within species of the genera Hanseniaspora and Kloeckera. FEMS Yeast Research. 1: 279–289.
Cheng CK, Demirci A, Catchmark MJ. 2011. Pullulan: Biosynthesis, production and applications. Applied Microbiology and Biotechnology. 92: 29–44.
Da?c? KE, D??rak M. 2005. Baz? meyve ekstraktlar?n?n antibakteriyal ve antifungal aktiviteleri. KSÜ Fen ve Mühendislik Dergisi 8 (2): 1-7.
De Curtis E, Torriani, S, Rossi E, De Cicco V. 1996. Selection and use of Metschnikowia Pulcherrima as a biological control agent for postharvest rots of peaches and table grapes. Annali de Microbiologia ed Enzymologia. 46: 45–55.
Delfini C, Formica JV. 2001. Wine microbiology science and technology. Marcel Dekker Inc., Italy.
Deshpande MS, Rale VB, Lynch JM. 1992. Aureobasidium pullulans in applied microbiology: A status report. Enzyme and Microbial Technology.14: 514–527.
Diaz MR, Fell JW. 2000. Molecular analysis of the IGS & ITS regions of rDNA of the psychrophilic yeasts in the genus Mrakia. Antonie van Leuwenhoek. 77: 7–12.
Dodor DE, Tabatabai MA. 2007. Arylamidase activity as an index of nitrogen mineralization in soils. Communications in Soil Science and Plant Analysis. 8: 2197-2207.
Esteve-Zarzoso B, Belloch C, Uruburu F, Querol A. 1999. Identification of Yeasts by RFLP analysis of the 5.8S rRNA gene and the two ribosomal internal transcribed spacers. International Journal of Systematic Bacteriology. 49: 329–337.
Felsenstein J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 39: 783-791.
Fleet GH, Charoenchai C, Henschke PA, Todd BEN. 1997. Screening of non-Saccharomyces wine yeasts for the presence of extracellular hydrolytic enzymes. Australian Journal of Grape Wine Research. 3: 2–8.
Garcia-Martos P, Marin P, Hernandez-Molina JM, Garcia-Agudo L, Aoufi S, Mira J. 2001. Extracellular enzymatic activity in 11 Cryptococcus species. Mycopathologia. 150: 1-4.
Gibson BR, Pham T, Wimalasena T, Box WG, Koivuranta K, Storgards E, Smart KA. 2011. Evaluation of ITS PCR and RFLP for differentiation and identification of brewing yeast and brewery ‘wild’ yeast contaminants. Journal of The Institute of Brewing. 117: 556–568.
Gonzalez SS, Barrio E, Querol A. 2007. Molecular identification and characterization of wine yeasts isolated from Tenerife (Canary Island, Spain). Journal of Applied Microbiology. 102(4): 1018-25. Doi: https://doi:10.1111/j.1365-2672.2006.03150.x
Gueguen Y, Chemardin P, Janbon G, Arnaud A, Galzy P. 1998. Investigation of the ?-glucosidases potentialities of yeast strains and application to bound aromatic terpenols liberation. Studies in Organic Chemistry. 53: 149–157.
Guillamon JM, Sabate J, Barrio E, Cano J, Querol A. 1998. Rapid identification of wine yeast species based on RFLP analysis of the ribosomal internal transcribed spacer (ITS) region. Archives of Microbiology. 169: 387–392.
Harhangi HR, Steenbakkers PJM, Akhmanova A, Jetten MSM, van der Drift C, Op den Camp HJM. 2002. A highly expressed family 1 ? -glucosidase with transglycosylation capacity from the anaerobic fungus Piromyces sp. E2. Biochimica et Biophysica Acta. 1574: 293–303.
Hierro N, Gonzalez A, Mas A, Guillamon JM. 2004. New PCR-based methods for yeast identification. Journal of Applied Microbiology. 97: 792–801. Doi:10.1111/j.1365-2672.2004.02369.x.
Johnson EA. 2013a. Biotechnology of non-Saccharomyces yeasts—the Ascomycetes Applied Microbiology and Biotechnology 97(2): 503–517. DOI: 10.1007/s00253-012-4497-y
Johnson EA. 2013b. Biotechnology of non-Saccharomyces yeasts—the Basidiomycetes Applied Microbiology and Biotechnology. 97(17): 7563–7577. DOI: 10.1007/s00253-013-5046-z
Karasova P, Spiwok V, Mala S, Kralova B, Russell NJ. 2002: Beta-galactosidase activity in psychrotrophic microorganisms and their potential use in food industry. Czech Journal of Food Sciences. 20: 43–47.
Keerti GA, Kumar V, Dubey A, Verma AK. 2014. Kinetic characterization and effect of immobilized thermostable ?-glucosidase in alginate gel Beads on sugarcane juice. ISRN Biochemistry, Article ID 178498, 8 Pages.
K?l?çgün H, Arda N, Uçar EÖ. 2015. Identification of longevity, fertility and growth-promoting properties of pomegranate in Caenorhabditis elegans. Pharmacognosy magazine. 11: 356–359.
Kreger-van Rij NJW. 1984. The yeast, a taxonomic study. Amsterdam, the Netherlands: Elsevier Science B.V.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35: 1547-1549.
Kurtzman CP, Fell JW. 1998. The yeasts: a taxonomic study, 4th edn. Amsterdam: Elsevier Science Publishers.
Kurtzman CP, Robnett CJ. 1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek. 73: 331–371.
Lee BH. 1996. Fundamentals of food biotechnology, VCH Publishers, USA.
Li D, Li X, Dang W, Tran PL, Park S, Oh B, Hong W, Lee J, Park K. 2013. Characterization and application of an acidophilic and thermostable ?-glucosidase from Thermofilum pendens. Journal of Bioscience and Bioengineering. 115(5): 490–496.
Liu HM, Guo JH, Cheng YJ, Luo L, Liu P, Wang BQ, Deng BX, Long CA. 2010a. Improvement of Hanseniaspora uvarum biocontrol activity against gray mold by the addition of ammonium molybdate and the possible mechanisms involved. Crop Protection. 29: 277–282.
Liu HM, Guo JH, Cheng YJ, Luo L, Liu P, Wang BQ, Deng BX, Long CA. 2010b Control of gray mold of grape by Hanseniaspora uvarum and its effects on postharvest quality parameters. Annals of Microbiology. 60: 31–35.
Lopez V, Querol A, Ramon D, Fernandez-Espinar MT. 2001. A simplified procedure to analyze mitochondrial DNA from industrial yeasts. International Journal of Food Microbiology. 68: 75–81.
Naumova ES, Korshunova IV, Jespersen L, Naumov GI. 2003. Molecular genetic identification of Saccharomyces sensu stricto strains for African sorghum beer. FEMS Yeast Research. 3: 177–184.
Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York.
Nikolaou E, Andrighetto C, Lombardi A, Nikolaos T. 2007. Heterogeneity in genetic and phenotypic characteristics of Saccharomyces cerevisiae strains isolated from red and white wine fermentations. Food Control 18: 1458–1465.
Nikolaou E, Soufleros EH, Boulompasi E, Tzanetakis N. 2006. Selection of indigenous Saccharomyces cerevisiae strains according to their oneological characteristics and vinification results. Food Microbiology. 23 (3): 205-211.
Piano S, Neyrotti V, Migheli Q., Gullino ML. 1997. Biocontrol capability of Metschnikowia pulcherrima against Botrytis postharvest rot of apple. Postharvest Biology and Technology. 11: 131–140.
Ramalho MT, Martin MAM, Cardoso MH, Queiroz MJ, Campos AMO. 1999. Biodegradation of azo dyes by the yeast Candida zeylanoides in batch aerated cultures. Chemosphere 38: 2455-2460.
Rodriguez-Vico F, Clemente-Jimenez JM, Mingorance-Cazorla L, Martinez-Rodriguez S, Las Heras-Vazquez FJ. 2003. Molecular characterization and oenological properties of wine yeasts isolated during spontaneous fermentation of six varieties of grape must. Food Microbiology. 21: 149–155.
Romano P, Capece A, Siesto G, Romaniello R. 2009. Restriction analysis of rDNA regions to differentiate non-Saccharomyces wine species in mixed cultures. Journal of Engineering and Technology Research. 1(4): 068-071.
Sabate J, Cano J, Esteve-Zarzoso B, Guillamon JM. 2002. Isolation and identification of yeast associated with Vineyard and winery by RFLP analysis of ribosomal genes and mitochondrial DNA. Microbiological Research. 157: 267–274.
Santos EV Martinez, AO, Munizaga GT, Reyes JE, Won MP. 2012. Effect of high hydrostatic pressure (HHP) processing on physicochemical properties, bioactive compounds and shelf-life of pomegranate juice. Innovative Food Science & Emerging Technologies. 13: 13–22.
Sena RF, Costelli MC, Gibson LH, Coughlin RW. 2006. Enhanced production of pullulan by two strains of A. pullulans with different concentrations of soybean oil in sucrose solution in batch fermentations. Brazilian Journal of Chemical Engineering. 23(4): 507–515.
Sevda SB, Rodrigues L, 2011. The making of pomegranate wine using yeast immobilized on sodium alginate. African Journal of Food Science. 5: 299–304.
Shaima S, Akram A, Halim SA, Tassaduq R, 2017. Sources of ? -galactosidase and its applications in food industry. 3 Biotechnology. 7 (1): 79. DOI 10.1007/s13205-017-0645-5.
Sherman F, Fink GR, Hicks JB. 1986. Methods in yeast genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
Spadaro D, Vola R, Piano S, Gullino ML. 2002. Mechanisms of action and efficacy of four isolates of the yeast Metschnikowia pulcherrima active against postharvest pathogens on apples. Postharvest Biology and Technology. 24: 123–134.
Török T, Rockhold D, King AD. 1993. Use of electrophoretic karyotyping and DNA-DNA hybridization in yeast identification. International Journal of Food Microbiology. 19: 63–80.
Vasiljevic T, Jelen P. 2001. Production of ?-galactosidase for lactose hydrolysis in milk and products using thermophilic lactic acid bacteria. Innovative Food Science & Emerging Technologies. 2: 75-85.
Vaughan Martini A, Martini A. 1987. Taxonomic revision of the yeast genus Kluyveromyces by nuclear deoxyribonucleic acid reassociation. International Journal of Systematic Bacteriology. 37 (4): 380–385.
Versavaud A, Hallet JN. 1995. Pulsed-Field gel electrophoresis combined with rare-cutting endonucleases for strain identification of Candida famata, Kloeckera apiculata and Schizosaccharomyces pombe with chromosome number and size estimation of the two former. Systematic and Applied Microbiology. 18: 303– 309.
Wang X, Li S, Yang X, Yang S, Zhu M. 2012. Technology prospecting on enzymes: application, Marketing and Engineering. 2(3): 1-11.
White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: A Guide to Methods and Applications Academic Press, San Diego, California, USA.
Yasoubi P, Barzegar M, Sahari MA, Azizi MH. 2007. Total phenolic contents and antioxidant activity of pomegranate (Punica granatum L.) peel extracts. Journal of Agricultural Science and Technology. 9: 35-42.