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Heterothallism of mucoraceous fungi: A review of biological implications and uses in biotechnology

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Abstract

The phenomenon of heterothallism in filamentous fungi is reviewed, with emphasis on the discussion of hormonal regulation of heterothallic strains of mucoraceous fungi. This process is viewed from the standpoint of current understanding that fungal cells communicate with each other using a special “language,” i.e., signaling chemicals (hormones or pheromones). Physiological and biochemical criteria of distinguishing between heterosexual strains, which make it possible to draw analogies with higher eukaryotes, are set forth for the first time, based on experimental data obtained with Blakeslea trispora. The synthetic pathway to trisporic acids (a zygogenic sex hormone of Mucorales), their relation to carotenoids, and biological functions are described. The similarity (both structural and functional) between fungal, plant, and animal hormones is another topic dealt with. Current understanding of the role of terpenoids in the evolution of sexual communication and transduction is presented with an excursion into microbial endocrinology, a novel field of research in biology. The concluding part of the review analyzes the data on biotechnological implications of the phenomenon of heterothallism. Specifically, it may be used to obtain a series of isoprenoid compounds, such as β-carotene and lycopene (which exhibit pronounced antioxidant activity), as well as sterols and trisporic acids.

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References

  1. Oleskin, A.V., Botvinko, I.V., and Tsavkelova, E.A., Mikrobiologiya, 2000, vol. 69, no. 3, pp. 309–327.

    CAS  Google Scholar 

  2. Voloshin, S.A. and Kaprel’yants, A.S., Biokhimiya, 2004, vol. 69, no. 11, pp. 1555–1564.

    Google Scholar 

  3. Tarchevskii, I.A., Signal’nye sistemy kletok rastenii (Signal Systems of Plant Cells), Moscow: Nauka, 2002.

    Google Scholar 

  4. Huxley, J.S., Biol. Rev., 1935, vol. 10, no. 3, pp. 427–441.

    CAS  Google Scholar 

  5. Raper, J.R., Bot. Rev., 1952, vol. 18, no. 3, pp. 427–441.

    Google Scholar 

  6. Gooday, G.W., in Hormone of Mycelial Fungi. The Mycota, Wessels, J.G.H. and Meinhardt, F., Eds., Berlin: Springer-Verlag, 1994, vol. 1, pp. 401–409.

    Google Scholar 

  7. Blakeslee, A.F., Proc. Natl. Acad. Sci. USA, 1904, vol. 40, no. 2, pp. 206–210.

    Google Scholar 

  8. Kursanov, M.I., Mikologiya (Mycology), Moscow: Gos. Uch.-Ped. Izd. Narkomprosa RSFSR, 1940.

    Google Scholar 

  9. Gooday, G.W, in Primitive Sensory and Communication Systemes, Esser, K. and Lemke, P.A., Eds., London: Academic, 1992, pp. 155–204.

    Google Scholar 

  10. Kothe, E., FEMS Microbiol. Lett., 1996, vol. 18, no. 1, pp. 65–87.

    Article  CAS  Google Scholar 

  11. Kellner, M., Burmester, F., Wostemeyer, A., and Wostmeer, J., Curr. Genetic, 1993, vol. 23, no. 2, pp. 334–337.

    Article  CAS  Google Scholar 

  12. Koltin, Y., Stamberg, J., and Lenke, P.A., Bacteriol. Rev., 1972, vol. 36, no. 2, pp. 156–171.

    PubMed  CAS  Google Scholar 

  13. Gooday, G.W., Ann. Rev. Biochem., 1972, vol. 43, no. 1, pp. 36–45.

    Google Scholar 

  14. Harold, F., The Vital Force. A Study of Bioenergetics, New York: Pergamon, 1986.

    Google Scholar 

  15. Kerwin, J.L. and Washino, R.K., Experiment. Mycol., 1983, vol. 7, no. 1, pp. 109–115.

    Article  CAS  Google Scholar 

  16. Sywichi, D., Vatenabe, M., and Yochimura, M., Arch. Microbiol., 1988, vol. 149, no. 5, pp. 507–508.

    Google Scholar 

  17. Kawai, G., Trans. Mycol. Soc. Japan, 1987, vol. 28, no. 1, pp. 107–119.

    Google Scholar 

  18. Flavier, A.B., Clough, S.J., Schell, M.A., and Denny, T.P., Mol. Microbiol., vol. 26, no. 2, pp. 251–259.

  19. Champel, S.P. and Elzayat, A.E., J. Bacteriol., 1989, vol. 171, no. 7, pp. 3982–3983.

    Google Scholar 

  20. Dyen, P.S., Ingraen, D.S., and Johnstone, K., Mycol. Res., 1993, vol. 97, no. 3, pp. 485–496.

    Google Scholar 

  21. Plasencia, I. and Mirocha, C.J., Phytopathology, 1990, vol. 8, no. 6, pp. 1019–1023.

    Google Scholar 

  22. Oleskin, A.V., Botvinko, I.V., and Kirovskaya, T.A., Vestnik MGU, 1998, issue 16, no. 4, pp. 3–10.

  23. Lenard, J., FEMS, 1992, vol. 17, no. 1, pp. 147–150.

    CAS  Google Scholar 

  24. Vunder, P.A., Andronov, E.V., and Andronova, T.A., Usp. Sovrem. Biol., 1999, vol. 119, no. 4, pp. 335–344.

    Google Scholar 

  25. Sandmann, G., Arch. Biochem. Biophys., 2001, vol. 385, no. 1, pp. 4–12.

    Article  PubMed  CAS  Google Scholar 

  26. Satina, S. and Blakeslea, A.G., Proc. Med. Acad. Sci, 1926, vol. 12, no. 1, pp. 191–196.

    Article  CAS  Google Scholar 

  27. Manoiloff, E.O., Müchene Mediziniche Wochtenschrift, 1929, no. 5, pp. 1784–1789.

  28. Feofilova, E.P., Consistent Patterns of Pigment Formation by Some Microorganisms in Relation to the Processes of Secondary Metabolism and Reproduction, Extended Abstract of Doctoral (Biol.) Dissertation, Moscow: INMI AN SSSR, 1978.

    Google Scholar 

  29. Smith, G., Trans British. Mycol. Ser., 1957, vol. 40, no. 3, pp. 481–498.

    Google Scholar 

  30. Feofilova, E.P., Tereshina, V.M., and Kochkina, G.A., Mikrobiologiya, 1997, vol. 66, no. 6, pp. 846–849.

    Google Scholar 

  31. Feofilova, E.P., Tereshina, V.M., and Memorskaya, A.S., Mikrobiologiya, 1997, vol. 66, no. 6, pp. 835–839.

    Google Scholar 

  32. Feofilova, E.P., Sadovova, N.V., and Mikhailova, M.M., Mikrobiologiya, 1993, vol. 62, no. 4, pp. 625–633.

    CAS  Google Scholar 

  33. Cagliotti, L., Canelli, J., Cunarino, B., Mandelli, R., and Prieto, A., Tetrahedron Supplement, 1966, no. 7, p. 175.

  34. Dedyukhina, E.G., A Study of Biosynthesis of Lipids in the Carotene-Forming Fungi V. trisrora, Cand. Sci. (Biol.) Dissertation, Moscow: INMI AN SSSR, 1969.

    Google Scholar 

  35. Thomas, D.M., Harris, R.C., Kirk, J.T.O., and Goodwin, T.W., Phytochemistry, 1967, vol. 6, no. 3, pp. 361–366.

    Article  CAS  Google Scholar 

  36. Yuldasheva, L.S., Feofilova, E.P., Samokhvalov, G.I., and Bekhtereva, M.N., Mikrobiologiya, 1972, vol. 41, no. 3, pp. 430–435.

    CAS  Google Scholar 

  37. Feofilova, E.P. and Pakhlavuni, I.K., Mikrobiologiya, 1972, vol. 43, no. 2, pp. 260–262.

    Google Scholar 

  38. Tereshina, V.M., Memorskaya, A.S., and Feofilova, E.P., Prikl. Biokhim. Mikrobiol., 2005, vol. 41, no. 4, pp. 449–453.

    PubMed  CAS  Google Scholar 

  39. Feofilova, E.P., Tereshina, V.M., and Memorskaya, A.S., Mikrobiologiya, 2005, vol. 74, no. 6, pp. 750–755.

    CAS  Google Scholar 

  40. Feofilova, E.P. and Kudryavtseva, N.N., Mikrobiologiya, 1974, vol. 43, no. 4, pp. 628–633.

    CAS  Google Scholar 

  41. Feofilova, E.P., Mikrobiologiya, 1970, vol. 39, no. 2, pp. 309–314.

    CAS  Google Scholar 

  42. Feofilova, E.P. and Arbuzov, V.A., Mikrobiologiya, 1975, vol. 44, no. 3, pp. 395–399.

    CAS  Google Scholar 

  43. Feofilova, E.P., Kudryavtseva, N.N., and Shakhova, I.K., Mikrobiologiya, 1974, vol. 43, no. 2, pp. 235–238.

    CAS  Google Scholar 

  44. Feofilova, E.P., Fateeva, T.V., and Arbuzov, V.A., Mikrobiologiya, 1976, vol. 45, no. 1, pp. 169–171.

    CAS  Google Scholar 

  45. Arbuzov, V.A., Feofilova, E.P., Ivanova, L.E., and Bekhtereva, M.N., Dokl. Akad. Nauk SSSR, 1976, vol. 226, no. 6, pp. 1449–1451.

    PubMed  CAS  Google Scholar 

  46. Bunbury, G.H., Nature, 1954, vol. 173, no. 4, p. 499.

    Article  Google Scholar 

  47. Plempel, M., Planta, 1960, vol. 55, pp. 120–128.

    Article  Google Scholar 

  48. Plempel, M. and David, W., Planta, 1961, vol. 56, p. 438.

    Article  Google Scholar 

  49. Cagliotti, L., Cainelli, G., Camerino, B., Mondelli, R., and Prieto, A., Chimica Ind., Milano, 1964, vol. 46.

  50. Ende, H. Van Den, Nature, 1967, vol. 215, no. 1, pp. 211–212.

    Article  PubMed  Google Scholar 

  51. Feofilova, E.P., Biol. Nauki, 1970, no. 1, pp. 115–123.

  52. Bergman, K., Burke, P.V., Cedra-Olmedo, E., David, C.N., Delbruck, M., Foster, K.W., Goodell, T.W., Heisenberg, M., Meissner, G., Zalokar, M., Dennison, D.S., and Shropshire, W., Bacterial. Rev., 1969, vol. 33, no. 1, pp. 99–157.

    CAS  Google Scholar 

  53. Austin, D.J., BuLock, J.D., and Drake, D., Experientia, 1970, vol. 26, no. 5, pp. 348–349.

    Article  PubMed  CAS  Google Scholar 

  54. BuLock, J.D. and Austin, D.J., Chem. Commun., 1970, no. 2, pp. 255–256.

  55. Gooday, G.W., Brian, E.D., and Wendy, H.L., FEBS, 1978, vol. 55, no. 2, pp. 221–229.

    CAS  Google Scholar 

  56. Gooday, G.W. and Gauger, W.L., Proc. I Inter. Congress I. A. M. S., Tokyo, 1975.

  57. Gessler, N.N., Sokolov, A.N., and Belozerskaya, T.A., Prikl. Biokhim. Mikrobiol., 2002, vol. 38, no. 6, pp. 625–639.

    PubMed  CAS  Google Scholar 

  58. Schwartz, S.H., Tan, B.C., Gage, D.A., Zeevaart, J.A.D., and Mc, Karty D.R., Science, 1997, vol. 276, no. 6, pp. 1872–1874.

    Article  PubMed  CAS  Google Scholar 

  59. Gessler, N.N., Sokolov, A.V, Bykhovskii, V.Ya., and Belozerskaya, T.A., Prikl. Biokhim. Mikrobiol., 2002, vol. 38, no. 3, pp. 237–242.

    PubMed  CAS  Google Scholar 

  60. Gessler, N.N., Sokolov, A.V., and Belozerskaya, T.A., Prikl. Biokhim. Mikrobiol., 2003, vol. 39, no. 4, pp. 427–429.

    Google Scholar 

  61. Guzhova, N.V., Varik, O.Ya., Rubin, L.B., and Fraikin, G.Ya., Mikol. Fitopatol., 1977, vol. 11, no. 6, pp. 467–471.

    CAS  Google Scholar 

  62. Feofilova, E.P., Dzhiembaev, B.Zh., Vakulova, L.A., Boltyanskaya, E.V., Sergeeva, L.N., Bekhtereva, M.N., and Samokhavlov, G.I., Biologich. Nauki, 1973, no. 5, pp. 96–99.

  63. Feofilova, E.P., Lozhnikova, V.N., Bekhtereva, M.N., Samokhvalov, G.I., and Chailakhyan, M.Kh., Dokl. Akad. Nauk SSSR, 1973, vol. 205, no. 3, pp. 433–435.

    Google Scholar 

  64. Feofilova, E.P. and Bekhtereva, M.N., Mikrobiologiya, 1976, vol. 45, no. 6, pp. 557–558.

    CAS  Google Scholar 

  65. Schimek, C., Kleppe, K., Saleem, A., Voigt, K., Burmester, A., and Wostemeyer, I., Mycol. Res., 2003, vol. 107, no. 6, pp. 736–747.

    Article  PubMed  CAS  Google Scholar 

  66. Drinkard, L.C., Nelson, G.E., and Sutter, R.P., Exp. Mycol., 1982, vol. 6, no. 1, pp. 52–59.

    Article  Google Scholar 

  67. Sutter, R. Dadok, J., Bothner-By, A., Smith, R., and Mishra, P., Biochemistry, 1989, vol. 28, pp. 4060–4066.

    Article  PubMed  CAS  Google Scholar 

  68. Sutter, R.P., Grandin, A., Dye, B., and Moore, W., Fungal Genet. Biol., 1996, vol. 20, no. 2, pp. 258–279.

    Google Scholar 

  69. Gooday, G., J. Gen. Microbiol., 1973, vol. 74, no. 1, pp. 233–239.

    CAS  Google Scholar 

  70. Gooday, G.W., Phil. Trans. R. Soc. Lond, 1978, vol. 284, no. 4, pp. 508–520.

    Google Scholar 

  71. Feofilova, E.P., Tereshina, V.M., and Vakulova, L.A., Mikrobiologiya, 1994, vol. 63, no. 1, pp. 17–22.

    CAS  Google Scholar 

  72. Feofilova, E.P., Mikrobiologiya, 1992, vol. 61, no. 5, pp. 741–789.

    CAS  Google Scholar 

  73. Rietz, P., Wiss, O., and Weber, F., Vitamins and Hormones, 1974, vol. 32, no. 2, pp. 237–249.

    PubMed  CAS  Google Scholar 

  74. Sutter, R., in Eukaryotic Microbes of model Developmental Systems, Day, D.H. and Horgen, P.A., eds., New York: Dekker, 1977.

    Google Scholar 

  75. Feofilova, E.P., Prikl. Biokhim. Mikrobiol., 2001, vol. 37, no. 2, pp. 141–155.

    PubMed  CAS  Google Scholar 

  76. Ostrovskii, M.A., Fotookislenie i patologiya zreniya. Svobodnye radikaly i antioksidanty v khimii i biologii (Photooxidation and Pathology of Vision. Free Radicals and Antioxidants in Chemistry and Biology), Moscow: Inst. Khim. Fiz. RAS, 2000.

    Google Scholar 

  77. Ciegler, A., Lagod, A., Sohns, V., and Jakson, R., Biotechnol. Bioeng.. 1963. V. 5. P. 109–121.

    Article  Google Scholar 

  78. Bekhtereva, M.N., Fiziologo-biokhimicheskoe izuchenie mikroorganizmov v svyazi s biosintezom biologicheski aktivnykh i drugikh soedinenii mikroorganizmov (Physiological and Biochemical Study of Microorganisms in Relation to Biosynthesis of Biologically Active and Other Compounds of Microorganisms), Moscow: INMIAN SSSR, 1973.

    Google Scholar 

  79. Heyes, Ph., Chichester, C.O., and Nakayama, T.O.M., Biochem. Biophys. Acta, 1964, vol. 90, no. 4, pp. 578–592.

    Google Scholar 

  80. Kolot, F.B. and Vakulova, L.A., Veselov, I.Ya., Samokhvalov G.I, Usp. Sovrem. Biol., 1971, vol. 71, no. 1, pp. 18–41.

    PubMed  CAS  Google Scholar 

  81. Ninet, L., Renaut, I., and Tissier, R., Biothechnol. Bioeng., 1969, vol. 9, no. 7, pp. 1196–1210.

    Google Scholar 

  82. Feofilova, E. P., Prikl. Biokhim. Mikrobiol., 1994, vol. 63, no. 1, pp. 17–23.

    CAS  Google Scholar 

  83. Feofilova, E.P., Ivanova, G.V., and Ushanova, A.G., Mikrobiologiya, 1982, vol. 51, no. 2, pp. 267–272.

    CAS  Google Scholar 

  84. Jeong, C., Biotechnol. Lett., 1999, vol. 21, no. 8, pp. 683–688.

    Article  CAS  Google Scholar 

  85. Chen Tao, Chen Zougeun, and Mu Youhua, Weishengwuxue Tongbao, 1998, vol. 25, no. 2, pp. 79–82.

    CAS  Google Scholar 

  86. Feofilova, E.P., Tereshina, V.M., Ivakin, A.F., and Kiseleva, A.I., Prikl. Biokhim. Mikrobiol., 1994, vol. 30, no. 3, pp. 415–419.

    CAS  Google Scholar 

  87. Rin, S.W., Lee, J.Y., Jeorg, J.C., Lee, J.H., and Park, Y.H., J. Microbiol. Biotechnol., 1999, vol. 9, no. 5, pp. 448–553.

    Google Scholar 

  88. Kim, S.-W., Seo, W.-T., and Park, Y.-H., Ferm. Bioeng., 1997, vol. 84, p. 23.

    Google Scholar 

  89. Metha, B.J. and Cerda-Olmedo, E., Appl. Microbiol. Biotechnol., 1955, vol. 42, no. 6, pp. 836–858.

    Google Scholar 

  90. Cerda-Olmedo, E., Biotechnology of Vitamines, Pigments and Growth Factors. III, London: Elsevier Appl. Sci, 1989, pp. 27–42.

    Google Scholar 

  91. RF Patent no. 2 177 505, Byull. Izobret., 2001.

  92. Bhosale, P., Appl. Microbiol. Biotechnol., 2004, vol. 63, no. 2, pp. 351–361.

    Article  PubMed  CAS  Google Scholar 

  93. Yager, H.K., US Patent no. 3 522 146, 1970.

  94. Finkelstein, M., Collins, F., Huang, C.C., Taiwan, T., Biang, G.S., Wash, W., Tsau, Bi-Ru, Hsien, T., and Leach, J., US Patent no. 5 328 845, 1994.

  95. BuLock, R.J. and Winstanley, D.J., J. Gen. Microbiol., 1971, vol. 69, no. 2, pp. 391–394.

    CAS  Google Scholar 

  96. Vakulova, L.A., Bayadzhan, G.A., Bekhtereva, M.N., and Samokhvalov, G.N., Dokl. Akad. Nauk SSSR, 1970, vol. 191, no. 3, pp. 696–698.

    PubMed  CAS  Google Scholar 

  97. Yuldasheva, L.S., Feofilova, E.P., Samokhavlov, G.I., and Bekhtereva, M.N., Mikrobiologiya, 1972, vol. 41, no. 3, pp. 30–435.

    Google Scholar 

  98. Pohar, K., Gong, M., Bahnson, R., Miller, E., and Clinton, S., World J. Urol., 2003, vol. 21, no. 1, pp. 9–18.

    PubMed  CAS  Google Scholar 

  99. Swarthout, E.J., US Patent no. 309 714, 1963.

  100. Avchiev, M.I., Deev, S.D., Butorova, I.Z., Zorina, L.V., and Avchieva, P.B., Biotekhnol., 2004, no. 1, pp. 76–81.

  101. RF Patent no. 2115678, Byull. Izobret., 1998.

  102. RF Patent no. 2166868, Byull. Izobret., 2001.

  103. Sandmann, G., Chem. Biol., 2003, vol. 10, no. 3, pp. 478–479.

    Article  PubMed  CAS  Google Scholar 

  104. Yamano, S. Ishii, T., Nakawaga, M., Ikenaga, H., and Misawa, N., Biosci. Biotechhol. Biochem., 1994, vol. 58, no. 6, pp. 1112–1114.

    Article  CAS  Google Scholar 

  105. Marin, V.J., Pitera, D.G., Wihers, S.T., Newman, J.D., and Kewasling, J.D., Nat. Biothechnol, 2003, vol. 21, no. 6, pp. 796–802.

    Article  CAS  Google Scholar 

  106. Umeno, D., Tobias, A., and Arnold, F., Microbiol. Mol. Biol. Rev., 2005, vol. 69, no. 1, pp. 51–78.

    Article  PubMed  CAS  Google Scholar 

  107. Linn, C.E., Campbell, M.J., and Roelovs, W.L., Science, 1987, vol. 237, no. 5, pp. 650–652.

    CAS  PubMed  Google Scholar 

  108. Shakirova, F.M., Allagulova, U.R., Bezrukova, M.V., and Gamalov, F.P., Dokl. Akad. Nauk 2005, vol. 420, no. 4, pp. 556–552.

    Google Scholar 

  109. Levinson, H.Z., Naturwissenschaften, 1972, vol. 59, no. 4, pp. 477–484.

    Article  PubMed  CAS  Google Scholar 

  110. Roth, J., LeRoth, D., Shiloach, J., Rosenzweig, J.L., Lesniak, M.A., and Havrankova, J., New England J. Med., 1982, vol. 306, no. 5, p. 532.

    Google Scholar 

  111. Gooday, G.W. and Adams, D.J., Adv. Microb. Physiol., 1993, vol. 34, no. 1, pp. 69–134.

    Article  PubMed  CAS  Google Scholar 

  112. Sergeev, A.Yu. and Sergeev, Yu.V., Gribkovye infektsii (Fungal Infections), Moscow: Binom, 2003.

    Google Scholar 

  113. Debabov, V.G., Mikrobiologiya, 1999, vol. 68, no. 6, pp. 823–833.

    CAS  Google Scholar 

  114. Avchieva, P.B., Buterova, I.A., and Avchiev, M.N., Eurasian Patent no. 002 468, 2002.

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Original Russian Text © E.P. Feofilova, 2006, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2006, Vol. 42, No. 5, pp. 501–519.

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Feofilova, E.P. Heterothallism of mucoraceous fungi: A review of biological implications and uses in biotechnology. Appl Biochem Microbiol 42, 439–454 (2006). https://doi.org/10.1134/S0003683806050012

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