Sex in the Rest: Mysterious Mating in the Chytridiomycota and Zygomycota

Alexander Idnurm; Timothy Y. James; Rytas Vilgalys

doi:10.1128/9781555815837.ch24

Chapter 24 : Sex in the Rest: Mysterious Mating in the Chytridiomycota and Zygomycota

Authors: Alexander Idnurm¹, Timothy Y. James², Rytas Vilgalys³

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 2: Department of Biology, Duke University, Durham, NC 27708; 3: Department of Biology, Duke University, Durham, NC 27708

Content Type: Monograph

Publication Year: 2007

Category: Fungi and Fungal Pathogenesis

Book DOI: 10.1128/9781555815837

Chapter DOI: 10.1128/9781555815837.ch24

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Sex in the Rest: Mysterious Mating in the Chytridiomycota and Zygomycota, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555815837/9781555814212_Chap24-1.gif /docserver/preview/fulltext/10.1128/9781555815837/9781555814212_Chap24-2.gif

Abstract:

This chapter discusses mating biology of basal fungi with emphasis on chytridiomycetes and zygomycetes. The chytrids and zygomycetes are ecologically diverse. Many of them are parasites, on hosts such as plants, algae, invertebrates, or other fungi. These nutritional requirements have precluded their isolation into axenic culture. Both chytrids and zygomycetes are capable of causing diseases in humans and other animals. A number of zygomycete fungi cause human diseases that are particularly difficult to treat with current antifungal agents. Most of the knowledge of sex in basal fungi comes from studies of behaviors of axenic cultures or careful observations made using light microscopy on natural substrates for the fungi. Chytridiomycetes have long been recognized to be divisible into several major groups based on life cycles and sexual mechanisms. Blastocladiales are exceptional among Fungi by having a life cycle with alternation of generations in which a diploid sporophyte can undergo extensive vegetative growth including asexual reproduction. The Zygomycota comprise nine orders, eight of which include species that undergo homothallic or heterothallic sex. Among the Zygomycota, the Mucorales are the best studied: it is generally inferred that similar patterns of mating occur in the other zygomycetes, although this may not be the case. Microsporidia are obligate intracellular parasites of animals (often insects) and humans, characterized by the absence or remnants of mitochondria and the presence of a specialized structure, the polar tube, with which they infect cells.

Citation: Idnurm A, James T, Vilgalys R. 2007. Sex in the Rest: Mysterious Mating in the Chytridiomycota and Zygomycota, p 407-418. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch24

Highlighted Text: Show | Hide

Full text loading...

Figures

Sex in the Rest: Mysterious Mating in the Chytridiomycota and Zygomycota

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815837.ch24-1,webId=/content/author/10.1128/9781555815837.ch24-1,properties={foaf_givenname=Alexander, foaf_name=Alexander Idnurm, foaf_surname=Idnurm, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815837.ch24-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815837.ch24-2,webId=/content/author/10.1128/9781555815837.ch24-2,properties={foaf_givenname=Timothy Y., foaf_name=Timothy Y. James, foaf_surname=James, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815837.ch24-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815837.ch24-3,webId=/content/author/10.1128/9781555815837.ch24-3,properties={foaf_givenname=Rytas, foaf_name=Rytas Vilgalys, foaf_surname=Vilgalys, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815837.ch24-aff3]]}]]

/content/10.1128/9781555815837.ch24.ch24fig01

Figure 24.1

A phylogenetic tree of the fungal kingdom, illustrating both diversity and ambiguity of relationships, with species discussed in the text listed. While some groups such as the Dikarya are well supported by phylogenetic studies, the relationships at the base of the tree remain ambiguous (represented by the thick line). Previously, taxa in gray have been classified as members of the Zygomycota and taxa in bold have been classified as members of the Chytridiomycota. Tree based on references 31 and 84 .

10.1128/9781555815837/f0408-01_thmb.gif

10.1128/9781555815837/f0408-01.gif

Figure 24.1

/content/10.1128/9781555815837.ch24.ch24fig02

Figure 24.2

Sexual and vegetative structures of zygomycetes and chytridiomycetes. (a through c) Mating and zygospore formation in the homothallic species Radiomyces spectabilis: fusion of undifferentiated gametangia; the arrow indicates septum delimiting one gametangium (a); young zygospore produced between two suspensors, only one of which is appendaged (arrow) (b); mature zygospore (c). (d) Asexual zoosporangium of Chytriomyces hyalinus subtended by filamentous rhizoids. (e) Resting spore of C. hyalinus. Arrows indicate the two empty zoospore cysts which presumably donated nuclei to the resting spore. (f) Thick-walled resting spores of Allomyces arbusculus.

10.1128/9781555815837/f0410-01_thmb.gif

10.1128/9781555815837/f0410-01.gif

Figure 24.2

/content/10.1128/9781555815837.ch24.ch24fig03

Figure 24.3

Diagram of the sexual cycle of the heterothallic fungus Phycomyces blakesleeanus (Mucorales, Zygomycota). Based on reference 12 .

10.1128/9781555815837/f0412-01_thmb.gif

10.1128/9781555815837/f0412-01.gif

Figure 24.3

Diagram of the sexual cycle of the heterothallic fungus Phycomyces blakesleeanus (Mucorales, Zygomycota). Based on reference 12 .

References

/content/book/10.1128/9781555815837.ch24

1. Alvarez, M. I.,, M. I. Peláez, and, A. P. Eslava. 1980. Recombination between ten markers in Phycomyces. Mol. Gen. Genet. 179: 447– 452.

2. Arrach, N.,, R. Fernández-Martín,, E. Cerdá-Olmedo, and, J. Avalos. 2001. A single gene for lycopene cyclase, phtoene synthase, and regulation of carotene biosynthesis in Phycomyces. Proc. Natl. Acad. Sci. USA 98: 1687– 1692.

3. Barnett, H. L.,, V. G. Lilly, and, R. F. Krause. 1956. Increased production of carotene by mixed + and - cultures of Choanephora cucurbitarum. Science 123: 141.

4. Benny, G. L.,, R. A. Humber, and, J. B. Morton. 2001. Zygomycota: Zygomycetes, p. 113–146. In D. J. McLaughlin,, E. G. McLaughlin, and, P. A. Lemke (ed.), The Mycota VIIA, Systematics and Evolution. Springer-Verlag, Berlin, Germany.

5. Blakeslee, A. F. 1904. Sexual reproduction in the Mucorineae. Proc. Am. Acad. Arts Sci. 40: 205– 319.

6. Burgeff,, H. 1924. Untersuchungen über Sexualität under Parasititismus bei Mucorineen. I. Bot. Abh. Heft 4: 5– 135.

7. Burgeff, H. 1914. Untersuchungen über Variabilität, Sexualität und Erblichkeit bei Phycomyces nitens Kuntze. Flora 107: 259– 316.

8. Bürglin, T. R. 2003. The homeobox genes of Encephalitozoon cuniculi (Microsporidia) reveal a putative mating-type locus. Dev. Genes Evol. 213: 50– 52.

9. Carlile,, M. J., and L. Machlis. 1965. The response of male gametes of Allomyces to the sexual hormone sirenin. Am. J. Bot. 52: 478– 483.

10. Cavalier-Smith, T. 2001. What are fungi?, p. 3–37. In P. A. Lemke (ed.), The Mycota, vol. 7A. Springer-Verlag, New York, NY.

11. Cerdá-Olmedo, E. 1974. Phycomyces, p. 343–357. In R. C. King (ed.), Handbook of Genetics. Plenum Press, New York, NY.

12. Cerdá-Olmedo, E. 2001. Phycomyces and the biology of light and color. FEMS Microbiol. Rev. 25: 503– 512.

13. Cerdá-Olmedo,, E. 1975. The genetics of Phycomyces blakesleeanus. Genet. Res. 25: 285– 296.

14. Chayakulkeeree, M.,, M. A. Ghannoum, and, J. R. Perfect. 2006. Zygomycosis: the re-emerging fungal infection. Eur. J. Clin. Microbiol. Infect. Dis. 25: 215– 229.

15. Couch, J. N. 1939. Heterothallism in the Chytridiales. J. Elisha Mitchell Sci. Soc. 55: 409– 414.

16. Czempinski,, K., V. Kruft,, J. Wöstemeyer, and A. Burmester. 1996. 4-Dihydromethyltrisporate dehydrogenase from Mucor mucedo, an enzyme of the sexual hormone pathway: purification, and cloning of the corresponding gene. Microbiology 142: 2647– 2654.

17. Díaz-Mínguez, J. M.,, M. A. López-Matas, and A. P. Eslava. 1999. Complementary mating types of Mucor circinelloides show electrophoretic karyotype heterogeneity. Curr. Genet. 36: 383– 389.

18. Doggett, M. S., and, D. Porter. 1996. Sexual reproduction in the fungal parasite, Zygorhizidium planktonicum. Mycologia 88: 720– 732.

19. Emerson, R. 1941. An experimental study on the life cycles and taxonomy of Allomyces. Lloydia 4: 77– 144.

20. Emerson,, R., and C. M. Wilson. 1954. Interspecific hybrids and the cytogenetics and cytotaxonomy of Euallomyces. Mycologia 46: 393– 434.

21. Eslava, A. P.,, M. I. Alvarez,, P. V. Burke, and, M. Delbrück. 1975. Genetic recombination in sexual crosses of Phycomyces. Genetics 80: 445– 462.

22. Eslava, A. P.,, M. I. Alvarez, and, M. Delbrück. 1975. Meiosis in Phycomyces. Proc. Natl. Acad. Sci. USA 72: 4076– 4080.

23. Feofilova, E. P. 2006. Heterothallism of Mucoraceous fungi: a review of biological implications and uses in biotechnology. Appl. Biochem. Microbiol. 42: 439– 454.

24. Fraser,, J. A., and J. Heitman. 2006. Sex, MAT, and the evolution of fungal virulence, p. 13–33. In J. Heitman,, S. G. Filler,, J. E. Edwards, Jr., and, A. P. Mitchell (ed.), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC.

25. Gauger, W. L. 1977. Meiotic gene segregation in Rhizopus stolonifer. J. Gen. Microbiol. 101: 211– 217.

26. Gooday,, G. W., and D. J. Adams. 1993. Sex hormones and fungi. Adv. Microb. Physiol. 34: 69– 145.

27. Hänfler, J.,, H. Teepe,, C. Weigel,, V. Kruft,, R. Lurz, and, J. Wöstemeyer. 1992. Circular extrachromosomal DNA codes for a surface protein in the (+) mating type of the zygomycete Absidia glauca. Curr. Genet. 22: 319– 325.

28. Harder, R., and, G. Sörgel. 1938. Über einen neuen planoisogamen Phycomyceten mit Generationswechsel und seine phylogenetische Bedeutung. Nachrichten Gesell. Wiss. Göttingen, Mat.-Physik Kl., Fachgruppe VI (Biol.) (N.F.) 3.

29. Hatch, W. R. 1938. Conjugation and zygote germination in Allomyces arbuscula. Ann. Bot. 2: 583– 614.

30. Hawksworth,, D. L. 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol. Res. 105: 1422– 1432.

31. James, T. Y.,, F. Kauff,, C. Schoch,, P. B. Matheny,, V. Hofstetter,, C. Cox,, G. Celio,, C. Gueidan,, E. Fraker,, J. Miadlikowska,, H. T. Lumbsch,, A. Rauhut,, V. Reeb,, A. E. Arnold,, A. Amtoft,, J. E. Stajich,, K. Hosaka,, G.-H. Sung,, D. Johnson,, B. O’Rourke,, M. Crockett,, M. Binder,, J. M. Curtis,, J. C. Slot,, Z. Wang,, A. W. Wilson,, A. Schüßler,, J. E. Longcore,, K. O’Donnell,, S. Mozley-Standridge,, D. Porter,, P. M. Letcher,, M. J. Powell,, J. W. Taylor,, M. M. White,, G. W. Griffith,, D. R. Davies,, R. A. Humber,, J. B. Morton,, J. Sugiyama,, A. Y. Rossman,, J. D. Rogers,, D. H. Pfister,, D. Hewitt,, K. Hansen,, S. Hambleton,, R. A. Shoemaker,, J. Kohlmeyer,, B. Volkmann-Kohlmeyer,, R. A. Spotts,, M. Serdani,, P. W. Crous,, K. W. Hughes,, K. Matsuura,, E. Langer,, G. Langer,, W. A. Untereiner,, R. Lücking, B. Büdel, D. M. Geiser,, A. Aptroot,, P. Diederich,, I. Schmitt,, M. Schultz,, R. Yahr,, D. Hibbett,, F. Lutzoni,, D. McLaughlin,, J. Spatafora, and, R. Vilgalys. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818– 822.

32. James, T. Y.,, P. M. Letcher,, J. E. Longcore,, S. E. Mozley-Standridge,, D. Porter,, M. J. Powell,, G. W. Griffith, and, R. Vilgalys. 2006. A molecular phylogeny of the flagellated Fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98: 860– 871.

33. Katinka, M. D.,, S. Duprat,, E. Cornillot,, G. Méténier, F. Thomarat,, G. Prensier,, V. Barbe,, E. Peyretaillade,, P. Brottier,, P. Wincker,, F. Delbac,, H. El Alaoui,, P. Peyret,, W. Saurin,, M. Gouy,, J. Weissenbach, and, C. P. Vivarès. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450– 453.

34. Kayser, T., and, J. Wöstemeyer. 1991. Electrophoretic karyotype of the zygomycete Absidia glauca: evidence for differences between mating types. Curr. Genet. 19: 279– 284.

35. Keeling, P. J. 2003. Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet. Biol. 38: 298– 309.

36. Kellner,, M., A. Bumester,, A. Wöstemeyer, and, J. Wöste-meyer. 1993. Transfer of genetic information from the mycoparasite Parasitella parasitica to its host Absidia glauca. Curr. Genet. 23: 334– 337.

37. Kirk, P. M.,, P. F. Cannon,, J. C. David, and, J. A. Staplers (ed.). 2001. Ainsworth & Bisby’s Dictionary of the Fungi, 9th ed. CAB International, Wallingford, United Kingdom.

38. Kneip, H. 1929. Allomyces jaranicus n. sp. ein anisogamer Phycomycet mit Planogameten. Ber. Dtsch. Bot. Ges. 47: 199– 212.

39. Kuzina,, V., and E. Cerdá-Olmedo. 2006. Modification of sexual development and carotene production by acetate and other small carboxylic acids in Blakeslea trispora and Phycomyces blakesleeanus. Appl. Environ. Microbiol. 72: 4917– 4922.

40. Liu, Y.,, M. Hodson, and, B. Hall. 2003. Heterozygosity in chytrids. Fungal Genet. Newsl. 50( Suppl.): 459.

41. Lorence, A., and, C. L. Nessler. 2004. Camptothecin, over four decades of surprising findings. Phytochemistry 65: 2735– 2749.

42. Lutzoni, F.,, F. Kauff,, C. J. Cox,, D. McLaughlin,, G. Celio,, B. Dentinger,, M. Padamsee,, D. Hibbett,, T. Y. James,, E. Baloch,, M. Grube,, V. Reeb,, V. Hofstetter,, C. Schoch,, A. E. Arnold,, J. Miadlikowska,, J. Spatafora,, D. Johnson,, S. Hambleton,, M. Crockett,, R. Shoemaker,, S. Hambleton,, M. Crockett,, R. Shoemaker,, G.-H. Sung,, R. Lücking, T. Lumbsch,, K. O’Donnell,, M. Binder,, P. Diederich,, D. Ertz,, C. Gueidan,, K. Hansen,, R. C. Harris,, K. Hosaka,, Y.-W. Lim,, B. Matheny,, H. Nishida,, D. Pfister,, J. Rogers,, A. Rossman,, I. Schmitt,, H. Sipman,, J. Stone,, J. Sugiyama,, R. Yahr, and, R. Vilgalys. 2004. Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am. J. Bot. 91: 1446– 1480.

43. Machlis, L. 1958. Evidence for a sexual hormone in Allomyces. Physiol. Plantarum 11: 181– 192.

44. Machlis,, L., W. H. Nutting, and, H. Rapoport. 1968. The structure of sirenin. J. Am. Chem. Soc. 90: 1674– 1676.

45. Machlis, L.,, W. H. Nutting,, M. W. Williams, and, H. Rapoport. 1966. Production, isolation, and characterization of sirenin. Biochemistry 5: 2147– 2152.

46. Mandai, T.,, K. Hara,, M. Kawada, and, J. Nokami. 1983. A new total synthesis of DL-sirenin. Tetrahedron Lett. 24: 1517– 1518.

47. Mehta, B. J., and, E. Cerdá-Olmedo. 2001. Intersexual partial diploids of Phycomyces. Genetics 158: 635– 641.

48. Michailides, T. J., and, R. A. Spotts. 1986. Mating types of Mucor piriformis isolated from soil and pear fruit in Oregon orchards. Mycologia 78: 766– 770.

49. Michielse, C. B.,, K. Salim,, P. Ragas,, A. F. J. Ram,, B. Kudla,, B. Jarry,, P. J. Punt, and, C. A. M. J. J. van den Hondel. 2004. Development of a system for integrative and stable transformation of the zygomycete Rhizopus oryzae by Agrobacterium-mediated DNA transfer. Mol. Genet. Genomics 271: 499– 510.

50. Miller, C. E., and, D. P. Dylewski. 1981. Syngamy and resting body development in Chytriomyces hyalinus (Chytridiales). Am. J. Bot. 68: 342– 349.

51. Moore, E. D., and, C. E. Miller. 1973. Resting body formation by rhizoidal fusion in Chytriomyces hyalinus. Mycologia 65: 145– 154.

52. Morehouse, E. A.,, T. Y. James,, A. R. Ganley,, R. Vilgalys,, L. Berger,, P. J. Murphy, and, J. E. Longcore. 2003. Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Mol. Ecol. 12: 395– 403.

53. Mullins, J. T. 1961. The life cycle and development of Dicytomorpha gen. nov. (formerly Pringsheimiella), a genus of the aquatic fungi. Am. J. Bot. 48: 377– 387.

54. Nicolás, F. E.,, S. Torres-Martínez, and, R. M. RuizVázquez. 2003. Two classes of small antisense RNAs in fungal RNA silencing triggered by non-integrative transgenes. EMBO J. 22: 3983– 3991.

55. Nielsen, T. A. B., and, L. W. Olson. 1982. Nuclear control of sexual differentiation in Allomyces macrogynus. Mycologia 74: 303– 312.

56. Nutting, W. H.,, H. Rapoport, and, L. Machlis. 1968. The structure of sirenin. J. Am. Chem. Soc. 90: 6434– 6438.

57. Obraztsova, I. N.,, N. Prados,, K. Holzmann,, J. Avalos, and, E. Cerdá-Olmedo. 2004. Genetic damage following introduction of DNA in Phycomyces. Fungal Genet. Biol. 41: 168– 180.

58. Ohnuki, T.,, Y. Etoh, and, T. Beppu. 1982. Intraspecific and interspecific hybridization of Mucor pusillus and Mucor miehei by protoplast fusion. Agric. Biol. Chem. 46: 451– 458.

59. Olson, L. W.,, T. A. B. Nielsen,, H. P. Heldt-Hansen, and, N. G. Grant. 1982. Maleness, its inheritance and control in the aquatic Phycomycete Allomyces macrogynus. Trans. Br. Mycol. Soc. 78: 331– 336.

60. Orejas, M.,, M. I. Peláez,, M. I. Alvarez, and, A. P. Eslava. 1987. A genetic map of Phycomyces blakesleeanus. Mol. Gen. Genet. 210: 69– 76.

61. Pommerville, J. 1982. Morphology and physiology of gamete mating and gamete fusion in the fungus Allomyces. J. Cell Sci. 53: 193– 209.

62. Pommerville,, J., and M. S. Fuller. 1976. The cytology of the gamete and fertilization of Allomyces macrogynus. Arch. Microbiol. 109: 21– 30.

63. Pommerville, J. C., and, L. W. Olson. 1987. Evidence for a male-produced pheromone in Allomyces macrogynus. Exp. Mycol. 11: 245– 248.

64. Pommerville, J. C.,, J. B. Strickland, and, K. E. Harding. 1990. Pheromone interactions and ionic communication in gametes of aquatic fungus Allomyces macrogynus. J. Chem. Ecol. 16: 121– 131.

65. Pommerville, J. C.,, J. B. Strickland,, D. Romo, and, K. E. Harding. 1988. Effects of analogs of the fungal sexual pheromone sirenin on male gamete motility in Allomyces macrogynus. Plant Physiol. 88: 139– 142.

66. Pounds, J. A.,, M. R. Bustamante,, L. A. Coloma,, J. A. Consuegra,, M. P. L. Fogden,, P. N. Foster,, E. La Marca,, K. L. Masters,, A. Merino-Viteri,, R. Puschendorf,, S. R. Ron,, G. A. Sánchez-Azofeifa,, C. J. Still, and, B. E. Young. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439: 161– 167.

67. Puri, S. C.,, V. Verma,, T. Amna,, G. N. Qazi, and, M. Spiteller. 2005. An endophytic fungus from Nothapodytes foetida that produces camptothecin. J. Nat. Prod. 68: 1717– 1719.

68. Remy, W.,, T. N. Taylor, and, H. Hass. 1994. Early Devonian fungi: Blastocladalean fungus with sexual reproduction. Am. J. Bot. 81: 690– 702.

69. Ribes, J. A.,, C. L. Vanover-Sams, and, D. J. Baker. 2000. Zygomycetes in human disease. Clin. Microbiol. Rev. 13: 236– 301.

70. Roncero, M. I. G., and, E. Cerdá-Olmedo. 1982. Genetics of carotene biosynthesis in Phycomyces. Curr. Genet. 5: 5– 8.

71. Sanz, C.,, M. I. Alvarez,, M. Orejas,, A. Velayos,, A. P. Eslava, and, E. P. Benito. 2002. Interallelic complementation provides genetic evidence for the multimeric organization of the Phycomyces blakesleeanus phytoene dehydrogenase. Eur. J. Biochem. 269: 902– 908.

72. Satina, S., and, A. F. Blakeslee. 1929. Criteria of male and female in bread moulds (Mucors). Proc. Natl. Acad. Sci. USA 15: 735– 740.

73. Schimek, C.,, K. Kleppe,, A.-R. Saleem,, K. Voigt,, A. Burmester, and, J. Wöstemeyer. 2003. Sexual reactions in Mortierellales are mediated by the trisporic acid system. Mycol. Res. 107: 736– 747.

74. Schimek, C.,, A. Petzold,, K. Schultze,, J. Wetzel,, F. Wolschendorf,, A. Burmester, and, J. Wöstemeyer. 2005. 4-Dihydromethyltrisporate dehydrogenase, an enzyme of the sex hormone pathway in Mucor mucedo, is constitutively transcribed but its activity is differently regulated in (+) and (−) mating types. Fungal Genet. Biol. 42: 804– 812.

75. Schultze, K.,, C. Schimek,, J. Wöstemeyer, and A. Burmester. 2005. Sexuality and parasitism share common regulatory pathways in the fungus Parasitella parasitica. Gene 348: 33– 44.

76. Seale, T. W., and, R. B. Runyan. 1979. Scanning electron microscopy of surface ultrastructure changes during meiosporangium maturation and meiospore liberation in the aquatic fungus Allomyces arbuscula. J. Bacteriol. 140: 276– 284.

77. Seif, E.,, J. Leight,, Y. Liu,, I. Roewer,, L. Forget, and, B. F. Lang. 2005. Comparative mitochondrial genomics in zygomycetes: bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms. Nucleic Acids Res. 33: 734– 744.

78. Sparrow, F. K. 1960. Aquatic Phycomycetes, 2nd ed. University of Michigan Press, Ann Arbor.

79. Stewart, N. J., and, B. L. Munday. 2005. Possible differences in pathogenicity between cane toad-, frog- and platypus-derived isolates of Mucor amphibiorum, and a platypus-derived isolate of Mucor circinelloides. Med. Mycol. 43: 127– 132.

80. Sutter, R. P. 1975. Mutations affecting sexual development in Phycomyces blakesleeanus. Proc. Natl. Acad. Sci. USA 72: 127– 130.

81. Sutter,, R. P., A. B. Grandin,, B. D. Dye, and, W. R. Moore. 1996. (−) mating type-specific mutants of Phycomyces defective in sex pheromone biosynthesis. Fungal Genet. Biol. 20: 268– 279.

82. Sykes, E. E., and, D. Porter. 1981. Meiosis in the aquatic fungus Catenaria allomycis. Protoplasma 105: 307– 320.

83. Tanabe, Y.,, M. Saikawa,, M. M. Watanabe, and, J. Sugiyama. 2004. Molecular phylogeny of Zygomycota based on EF-1a and RPB1 sequences: limitations and utility of alternative markers to rDNA. Mol. Phylogenet. Evol. 30: 438– 449.

84. Tanabe, Y.,, M. M. Watanabe, and, J. Sugiyama. 2005. Evolutionary relationships among basal fungi (Chytridiomycota and Zygomycota): insights from molecular phylogenetics. J. Gen. Appl. Microbiol. 51: 267– 276.

85. Tehler, A.,, J. S. Farris,, D. L. Lipscomb, and, M. Kallersjo. 2000. Phylogenetic analyses of the fungi based on large rDNA data sets. Mycologia 92: 459– 474.

86. Torres-Martínez, S.,, F. J. Murillo, and, E. Cerdá-Olmedo. 1980. Genetics of lycopene cyclization and substrate transfer in beta-carotene biosynthesis in Phycomyces. Genet. Res. 36: 299– 309.

87. Whisler, H. C.,, S. L. Zebold, and, J. A. Shemanchuk. 1975. Life history of Coelomomyces psorophorae. Proc. Natl. Acad. Sci. USA 72: 693– 696.

88. White, M. M.,, T. Y. James,, K. O’Donnell,, M. Cafaro,, Y. Tanabe, and, J. Sugiyama. 2006. Phylogeny of the Zygomycota based on nuclear ribosomal sequence data. Mycologia 98: 872– 884.

89. Wöstemeyer, A.,, H. Teepe, and, J. Wöstemeyer. 1990. Genetic interactions in somatic inter-mating type hybrids of the zygomycete Absidia glauca. Curr. Genet. 17: 163– 168.

90. Wöstemeyer, J., and, E. Brockhausen-Rohdemann. 1987. Inter-mating type protoplast fusion in the zygomycete Absidia glauca. Curr. Genet. 12: 435– 441.

91. Wöstemeyer, J.,, A. Wöstemeyer, A. Burmester, and, K. Czempinski. 1995. Relationships between sexual processes and parasitic interactions in the host-pathogen system Absidia glauca-Parasitella parasitica. Can. J. Bot. 73( Suppl. 1): S243– S250.

92. Wubah, D. A.,, M. S. Fuller, and, D. E. Akin. 1991. Resistant body formation in Neocallimastix sp., an anaerobic fungus from the rumen of a cow. Mycologia 83: 40– 47.

93. Wurtz, T., and, H. Jockusch. 1978. Morphogenesis in Mucor mucedo: mutations affecting gamone response and organ differentiation. Mol. Gen. Genet. 159: 249– 257.

94. Wurtz, T., and, H. Jockusch. 1975. Sexual differentiation in Mucor: trisporic acid response mutants and mutants blocked in zygospore development. Dev. Biol. 43: 213– 220.