Abstract
The recent data on the pathways of carotenoid biosynthesis, which resulted in revision of the earlier concepts, are analyzed. Trisporoid diversity and their role in the sexual process of mucoraceous fungi, resulting in formation of sexual cells (zygospores) are discussed. Special attention is paid to the role of trisporic acids in carotenogenesis of combined culture of the (+) and (−) strains, in which zygospores are not formed.
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Medina, H.R., Cerdá-Olmedo, E., and Al-Babili, S., Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces, Mol. Microbiol., 2011, vol. 82, no. 1, pp. 199–208.
Gooday, G.W., Functions of trisporic acid, Phil. Trans. R. Soc. Lond. B, 1978, vol. 284, pp. 509–520.
Schimek, C., Kleepe, K., Saleem, A.-R., Voigt, K., and Burmester, A., and Wöstmeyer, J., Sexual reactions in Mortierellales are mediated by the trisporic acid system, Mycol. Res., 2003, vol. 107, no. 6, pp. 736–747.
Wöstemeyer, J., Wöstemeyer, Burmester, A., and Czempinski, K., Relationships between sexual processes and parasitic interactions in the host-pathogen system Absidia glauca — Parasitella parasitica, Can. J. Bot., 1995, vol. 73, pp. 243–250.
Schimek C. and Wöstmeyer, J., Pheromone action in the fungal groups Chytridiomycota and Zygomycota, and in the Oomycota in The Mycota. I Growth, Differentiation and Sexuality, Fischer, R. and Kües, U. Eds., Berlin: Springer, 2006, pp. 215–232.
Werkman, B.A. and Ende, H., Trisporic acid synthesis in homothallic and heterothallic mucorales, J. Gen. Microbiol., 1974, vol. 82, pp. 273–278.
Feofilova, E.P., Heterothallism of mucoraceous molds: a review of biological implications and the uses in biotechnology, Appl. Biochem. Microbiol., 2006, vol. 42, no. 5, pp. 501–519.
Krinsky, N.I., The biological properties of carotenoids, Pure Appl. Chem., 1994, vol. 66, no. 5, pp. 1003–1010.
Gann, P.H., Ma, J., Giovannucci, E., Willett, W., Sacks, F.M., Hennekens, C.H., and Stampfer, M.J., Lower prostate cancer risk in men with elevated plasma lycopene levels: results of a prospective analysis, Cancer Res., 1999, vol. 59, no. 6, pp. 1125–1230.
Tanaka, T., Shnimizu, M., and Moriwaki, H., Cancer chemoprevention by carotenoids, Molecules, 2012, vol. 17, no. 3, pp. 3202–3242.
Feofilova, E.P., Mycelial fungi as potential sources of new drugs with immunomodulatry, anti-tumor and wound-healing properties, Int. J. Immunopathol., Allergol., Infectol., 2004, vol. 1, pp. 27–33.
Bekhtereva, M.N. Physiological and biochemical investigation of microorganisms associated with biosynthesis of the biologically active and other compounds, Extended Abstract of doctoral (Biol.) Dissertation, Moscow: Institute of Microbiology. Russ. Acad. Sci., 1973.
Feofilova, E.P., Tereshina, V.M., and Memorskaya, A.S., RF Patent no. 2115678, 1998.
Feofilova, E.P., Tereshina, V.M., Memorskaya, A.S, Vakulova, L.A., and Shashkina, M.Ya., RF Patent no. 2166868, 2001.
Austin, D.J., Bu’Lock, J.D., and Drake, D., The biosynthesis of trisporic acids from β-carotene via retinal and trisporol, Experientia, 1970, vol. 26, no. 4, pp. 348–349.
Werkman, B.A. and van den Ende, H., Trisporic acid synthesis in Blakeslea trispora. Interaction between plus and minus mating types, Arch. Microbiol., 1973, vol. 90, pp. 365–374.
Bu’Lock, J.D., Jones, B.E., Taylor, D., Winskill, N., and Quarrie, S.A., Sex hormones in Mucorales. The incorporation of C20 and C18 precursors into trisporic acids, J. Gen. Microbiol., 1974, vol. 80, pp. 301–306.
Sutter, R.P. and Rafelson, M.E., Separation of β-factor synthesis from stimulated β-carotene synthesis in mated cultures of Blakeslea trispora, J. Bacteriol., 1968, vol. 95, no. 2, pp. 426–432.
Sutter, R.P., Trisporic acid synthesis in Blakeslea trispora, Science, 1970, vol. 168, pp. 1590–1592.
Sutter, R.P., Harrison, T.L., and Galasko, G., Trisporic acid biosynthesis in Blakeslea trispora via mating type-specific precursors, J. Biol.Chem., vol. 249, no. 7, pp. 2282–2284.
Schachtschabel, D. and Boland, W., Efficient generation of a trisporoid library by combination of synthesis and biotransformation, Org. Chem., 2007, vol. 72, no. 4, pp. 1366–1372.
Sutter, R.P., Capage, D.A., Harrison, T.L., and Keen, W.A., Trisporic acid biosynthesis in separate plus and minus cultures of Blakeslea trispora: identification by Mucor assay of two mating-type-specific components, J. Bacteriol., 1973, vol. 114, no. 3, pp. 1074–1082.
Schachtschabel, D., David, A., Menzel, K., Schimek, C., Wöstemeyer, J., and Boland, W., Cooperative biosynthesis of trisporoids by the (+) and (−) mating types of the zygomycete Blakeslea trispora, Chem. Biol. Chem., 2008, vol. 9, no. 18, pp. 3004–3012.
Polaino, S., Gonzalez-Felgado, J.A., Arteaga, P., Herrador, M.M., Barrero, A.F., and Cerdá-Olmedo, E., Apocarotenoids in the sexual interaction of Phycomyces blakesleeanus, Org. Biomol. Chem, 2012, vol. 10, pp. 3002–3009.
Polaino, S., Herrador, M.M., Cerdá-Olmedo, E., and Barrero, A.F., Splitting of β-carotene in the sexual interaction of Phycomyces, Org. Biomol. Chem, 2010, vol. 8, pp. 4229–4231.
Sutter, R.P., Apotrisporin-E: a new sesquiterpenoid isolated from Phycomyces blakesleeanus and Blakeslea trispora, Exp. Mycol., 1986, vol. 10, pp. 256–258.
Sutter, R.P. and Zawodny, P.D., Apotrisporine: a major metabolite of Blakeslea trispora, Exp. Mycol., 1984, vol. 8, pp. 89–92.
Sutter, R.P. and Whitaker, J.P., Zygophore-stimulating precursors (pheromones) of trisporic acids active in (==)-Phycomyces blakesleeanus, J. Biol, Chem, 1981, vol. 256, no. 5, pp. 2334–2341.
Schimek, C. and Wöstemeyer, J., Carotene derivatives in sexual communication of zygomycete fungi, Phytochemistry, 2009, vol. 70, pp. 1867–1875.
Gessler, N.N., Sokolov, A.V., Bykhovskii, V.Ya., and Belozerskaya, T.A., Superoxide dismutase and catalase activities in carotenoid-synthesizing fungi Blakeslea trispora and Neurospora crassa in oxidative stress, Appl. Biochem. Microbiol., 2002, vol. 38, no. 3, pp. 237–242.
Gomboeva, S.B., Gessler, N.N., Shumaev, K.B., Khomich, T.I., Moiseenok, A.G., and Bykhovskii, V.Y., Some natural and synthetic antioxidants as stabilizers of β-carotene conversion into vitamin A, Biochemistry (Moscow), 1998, vol. 63, no. 2, pp. 185–190.
Schachtschabel, D., Menzel, K.-D., Krauter, G., David, A., Roth, M., Horn, U., Boland, W., Wöstemeyer, J., and Schimek, C., Production and derivate composition of trisporoids in extended fermentation of Blakeslea trispora, Appl. Microbiol. Biotechnol., 2010, vol. 88, pp. 241–249.
Schachtschabel, D. Schimek, C., Wöstemeyer, J., and Boland, W., Biological activity of trisporoid analogues in Mucor mucedo, Phytochemistry, 2005, vol. 66, pp. 1358–1365.
Sutter, R.P., Dadok, J., Bothner-By, A.A., Smith, R.R., and Mishra, P.K., Cultures of separating mating types of Blakeslea trispora make D and E forms of trisporic acids, Biochemistry, 1989, vol. 28, pp. 4060–4066.
Bu’Lock, J.D., Jones, B.E., and Winskill, N., The apocarotenoid system of sex hormones and prohormones in Mucorales, Pure Appl. Chem., 1976, vol. 47, pp. 191–202.
Ende, H., Wiechmann, A.H.C.A., Reyngoud, D.J., and Hendriks, T., Hormonal interactions in Mucor mucedo and Blakeslea trispora, J. Bacteriol., 1970, vol. 101, no. 2, pp. 423–428.
Nieuwenhuis, M. and Ende, H., Sex specificity of hormone synthesis in Mucor mucedo, Arch. Microbiol., 1975, vol. 102, pp. 167–169.
Miller, M.L. and Sutter, R.P., Methyl trisporate E, J. Biol., Chem., 1984, vol. 259, no. 10, pp. 6420–6422.
Burgeff, H., Untersuchungen über Sexualitöt und Parasitismus bei Mucorineen, Fisher, G., Ed., Gena, 1924.
Vereshchagina, O.A., Memorskaya, A.S., Kochkina, G.A., and Tereshina, V.M., Trisporoids and carotenoids in Blakeslea trispora strains differing in capacity for zygote formation, Microbiology (Moscow), 2012, vol. 81, no. 5, pp. 526–533.
Schlicht, M., Šamajovcuso, S., Menzel, D., Boland, W., and Baluška, F., D’orenon blocks polarized tip growth of root hairs by interfering with the PIN2-mediated auxin transport network in the root apex, The Plant J., 2008, vol. 55, pp. 709–717.
Burmester, A., Richter, M., Schultze, K., Voelz, K., Schachtschabel, D., Boland, W., Wöstemeyer, J., and Schimek, C., Cleavage of β-carotene as the first step in sexual hormone synthesis in Zygomycetes is mediated by a trisporic acid regulated β-carotene oxygenase, Fungal Genet. Biol., 2007, vol. 44, pp. 1096–1108.
Tagua, V.G., Medina, H.R., Martín-Domínguez, R., Eslava, A.P., Corrochano, L.M., Cerdá-Olmedo, E., and Idnurm, A., A gene for carotene cleavage required for pheromone biosynthesis and carotene regulation in the fungus Phycomyces blakesleeanus, Fungal Genet. Biol, 2012, vol. 49, pp. 398–404.
Govind, N.S., Amin, A.R., and Modi, V.V., Stimulation of carotenogenesis in Blakeslea trispora, Phytochemistry, 1982, vol. 21, no. 5, pp. 1043–1044.
Shmidt, A., Heinecamp, T., Matuschek, M., Liebmann, B., Bollschweiler, C., and Brakhage, A.A., Analysis of mating-dependent transcription of Blakeslea trispora carotenoid biosynthesis genes carB and carRA by quantitative real-time PCR, Appl.Microbiol. Biotechno, 2005, vol. 67, no. 4, pp. 549–555.
Wetzel, J., Scheibner, O., Burmester, A., Schimek, C., and Wöstemeyer, J., 4-Dihydrotrisporindehydrogenase, an enzyme of sex hormone pathway of Mucor mucedo: purification, cloning of the corresponding gene, and developmental expression, Eukaryotic Cell, 2009, vol. 8, no. 1, pp. 88–95.
Schimek, C., Petzold, A., Schultze, K., Wetzel, J., Wolschendorf, F., Burmester, A., and Wöstmeyer, J., 4-Dihydromethyltrisporate dehydrogenase, an enzyme of sex hormone pathway in Mucor mucedo, is constitutively transcribed but its activity is differently regulated in (+) and (−) mating types, Fungal Genet. Biol., 2005, vol. 42, pp. 804–812.
Chempinski, K. and Kruft, V., Wöstemeyer, J., and Burmester, A., 4-Dihydro-methyltrisporate dehydrogenase from Mucor mucedo, an enzyme of the sexual hormone pathway: purification, and cloning of the corresponding gene, Arch. Microbiol., 1996, vol. 142, no. 9, pp. 2647–2654.
Ellenberger, S. and Schuster, S., and Wöstemeyer, J., Correlation between sequence, structure and function for trisporoid processing proteins in the model zygomycete Mucor mucedo, J. Theoret. Biol., vol. 320, pp. 66–75.
Werkman, B.A., Localization and partial characterization of a sex-specific enzyme in homothallic and heterothallic mucorales, Arch. Microbiol., vol. 109, no. 3, pp. 209–213.
Feofilova, E.P., Tereshina, V.M., Lokshin, B.V., Oreshkin, A.E., and Ivanova, N.I., The effect of trisporic acids on the composition of components of the cell wall in Blakeslea trispora Thaxter, Mikrobiologiia, 1977, vol. 46, no. 5, pp. 938–943.
Tereshina, V.M. and Feofilova, E.P., Effect of trisporic acids on Cunninghamella japonica cell wall composition, Mikrobiologiia, 1980, vol. 49, no. 1, pp. 172–174.
Blakeslee, A.F. and Cartlege, J.L., Sexual dimorphism in Mucorales. Interspecies reactions, Bot. Gaz., 1927, vol. 84, pp. 51–57.
Cross, F., Conjugation in Saccharomyces cerevisiae, Annu. Rev. Cell Biol., 1988, vol. 4, pp. 429–457.
Vereshchagina, O.A., Memorskaya, A.S., and Tereshina, V.M., Trisporoids under the stimulation of carotenogenesis in Blakeslea trispora, Microbiology (Moscow), 2012, vol. 81, no. 5, pp. 517–525.
Idnurm, A., Walton, F.J., Floyd, A., and Heitman, J., Identification of the sex genes in an early diverged fungus, Nature, 2008, vol. 451, pp. 193–196.
Grydanskyi, A.P., Lee, S.C., Litvintseva, A.P., Smith, M.E., Bonito, G., Porter, T.M., Anishchenko, I.M., Heitman, J., and Vilgalys, R., Structure, function, and phylogeny of the mating locus in the Rhyzopus orizae complex, Plos One, 2010, vol. 5, no. 12, pp. 1–12.
Wetzel, J., Burmester, A., Kolbe, M., and Wöstemeyer, J., The mating-related loci sexM and sexP of the zygomycetous fungus Mucor mucedo and their transcriptional regulation by trisporoid pheromones, Arch. Microbiol., 2012, vol. 158, pp. 1016–1023.
Mathur, N. and Sabhoy, A.K., Correlation between β-carotene content, several physical factors and the formation of zygospores in Mucor spp., Microbiol. Res., 1999, vol. 154, pp. 137–143.
Tereshina, V.M., Memorskaya, A.S., and Feofilova, E.P., MZygote formation in Blakeslea trispora: morphological peculiarities and relationship with carotenoid synthesis, Microbiology (Moscow), 2003, vol. 72, no. 4, pp. 27–33.
Morozova, E.S., Vasil’chenko, L.G., Ryazanova, E.M, Kiseleva, A.I., Panova, N.A., and Voronova, N.V., 1996, RF Patent no. 2053301.
Sutter, R.P., Grandin, A.B., Dye, B.D., and Moore, W.R., (−) Mating type-specific mutants of Phycomyces defective in sex pheromone biosynthesis, Fungal Gen. Biol., 1996, vol. 20, no. 4, pp. 268–279.
Bhosale, P., Environmental and cultural stimulants in the production of carotenoids from microorganisms, Appl. Microbiol. Biotechnol., 2004, vol. 63, no. 4, pp. 351–361.
Goldstein, J. and Brown, M.S., Regulation of the mevalonate pathway, Nature, 1990, vol. 343, no. 1, pp. 425–430.
Lampila, L.E., Wallen, S.E., and Bullerman, L.B., A review of factors affecting biosynthesis of carotenoids by order Mucorales, Mycopathol., 1985, vol. 90, pp. 65–80.
Ninet, L., Renault, J., and Tissier, R., Activation of the biosynthesis of carotenoids by Blakeslea trispora, Biotech. Bioeng., 1969, vol. 11, pp. 1195–1210.
Van den Ende, H., Relationship between sexuality and carotene synthesis in Blakeslea trispora, J. Bacteriol., 1968, vol. 96, no. 4, pp. 1298–1303.
Feofilova, E.P. and Bekhtereva, M.N., Effect of vitamin A on the biosynthesis of carotene by Blakeslea trispora, Mikrobiologiia, 1976, vol. 45, no. 3, pp. 557–558.
Filkenstein, M., Huang, C.-C., Bynh, G.S., Tsau, B.-R., and Leach, J., Fungal negative microorganism capable of producing high level of beta-carotene, US Patent, 1994, no. 328845.
Feofilova, E.P., Pigmenty mikroorganizmov. (Pigments of Microorganisms), Moscow: Nauka, 1974.
Kalinina, N.V., Tereshina, V.M., Memorskaya, A.S., and Feofilova, E.P., The correlation between the synthesis of β-carotene and zygote formation by Blakeslea trispora heterothallic strains, Appl. Biochem. Microbiol., 2007, vol. 43, no. 1, p. 68–72.
Rao, S. and Modi, V.V., Carotenogenesis: possible mechanism of action of trisporic acid in Blakeslea trispora, Experientia, 1977, vol. 33, no. 1, pp. 31–33.
Thomas, D.M., Harris, R.C., Kirk, J.T.O., and Goodwin, T.W., Studies on carotenogenesis in Blakeslea trispora—II. The mode of action of trisporic acid, Phytochemistry, 1967, vol. 6, pp. 361–366.
Feofilova, E.P. and Arbuzov, V.A., Mechanism of action of beta-ionone on the carotene-synthesizing enzymes of Blakeslea trispora, Mikrobiologiia, 1975, vol. 44, no. 3, pp. 395–399.
Feofilova, E.P., Tereshina, V.M., and Memorskaya, A.S., Regulation of lycopene biosynthess in mucorous fungus Blakeslea trispora by pyridine derivatives, Mikrobiologiia, 1995, vol. 64, no. 6, pp. 734–740.
Bouvier, F., d’Harlingue, A., and Camara, B., Molecular analysis of carotenoid cyclase inhibition, Arch. Biochem. Biophys., 1997, no. 1, pp. 53–64.
Reyes, P., Chichester, C.O., and Nakayama, T.O.M., The mechanism of β-ionone stimulation of carotenoid and ergosterol biosynthesis in Phycomyces blakesleeanus, Biochim. Biophys. Acta, 1964, vol. 90, pp. 578–592.
Bu’Lock, J.D. and Winstanley, D.J., Trisporic acid production by Blakeslea trispora and its promotion by barbiturate, J. Gen. Microbiol., 1971, vol. 69, pp. 391–394.
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Vereshchagina, O.A., Tereshina, V.M. Trisporoids and carotenogenesis in Blakeslea trispora . Microbiology 83, 438–449 (2014). https://doi.org/10.1134/S0026261714050270
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DOI: https://doi.org/10.1134/S0026261714050270