Choanephoraceae
Overview
The Choanephoraceae initially contained only a single genus, Choanephora (Schröter, 1893). However, later authors (Zycha et al., 1969; Hesseltine and Ellis, 1973) included several unrelated genera in the family: Cokeromyces, Cunninghamella, Gilbertella, Mycotypha and Radiomyces (Mucorales), and Rhopalomyces, Sigmoideomyces and Thamnocephalis (Zoopagales). On occasion, Choanephora was placed in other mucoralean families including Chaetocladiaceae (Lendner, 1908) and Thamnidiaceae (Pidoplichko and Mil’ko, 1971; Mil’ko, 1974). Most contemporary treatments of the family included two genera, Blakeslea and Choanephora, or the latter genus alone, if Blakeslea was considered a synonym of Choanephora (Hesseltine, 1955; Benjamin, 1959, 1979).
Kirk (1984) monographed the Choanephoraceae and recognized three genera, Blakeslea, Choanephora and a new genus, Poitrasia, based upon Blakeslea circinans. Papp et al. (2003) discussed the phylogenetic relationship of Blakeslea, Choanephora, Gilbertella and Poitrasia and six members of the Mucoraceae from Mucor and Rhizomucor. This analysis was based on a data set composed of ITS1, ITS2, and 5.8S sequences. Papp et al. (2003) considered Gilbertella (Gilbertellaceae) intermediate between Blakeslea, Choanephora and Poitrasia (Choanephoraceae) and the Mucoraceae. Later, Voigt and Olsson (2008), using maximum parsimony and distance, analyzed a multigene (act, ref-1a, 18S rRNA, 28S rRNA) data set obtained from selected species of 50 genera of the Mucorales. The results of their analysis clearly demonstrate that Gilbertella should be included in the Choanephoraceae based on 100% and 98% bootstrap values. Voigt and Olsson’s (2008) four-genus concept of the Choanephoraceae is being followed here. Cannon and Kirk (2007) and Kirk et al. (2008) also recognize a Choanephoraceae that includes the four genera of Voigt and Olsson (2008).
Members of the Choanephoraceae have a number of distinctive characteristics when one considers both the anamorph and teleomorph. If only the anamorphs are available, Gilbertella and other Choanephoraceae, can be distinguished by cultural characteristics. Gilbertella persicaria (Eddy) Hesseltine will sporulate after repeated transfer on most laboratory media, whether rich or poor in nutrients, whereas the other three genera of Choanephoraceae, Blakeslea, Choanephora and Poitrasia, will sporulate only on nutrient-poor media. Gilbertella and Poitrasia lack sporangiola whereas the other two genera of Choanephoraceae, Blakeslea and Choanephora, produce both sporangia and sporangiola. If zygospores can be induced in culture, species of Blakeslea, Choanephora and Poitrasia produce a very characteristic type borne on apposed suspensors that has a smooth, hyaline, zygosporangium and a pigmented, striate zygospore. Gilbertella persicaria, on the other hand, produces a typical Mucor-type zygospore with opposed suspensors, a rough, pigmented zygosporangium, and a hyaline, smooth-walled zygospore.
Classically, Blakeslea and Choanephora were distinguished from one another because of the formation of unispored (Choanephora) vs. multispored (Blakeslea) sporangiola. Poitras (1955) argued for combining these genera because the so-celled “conidia” of Choanephora spp. were in reality unispored sporangiola whose wall was not readily separable from the sporangiospore wall. Sporangiospores with apical hyaline appendages are produced by all members of the Choanephoraceae. A second species of Blakeslea, B. monospora B.S. Mehrotra & Baijal (1968), was described that produces one- and two-spored sporangiola in which the sporangiolar wall is readily separable from the spore wall in the unispored sporangiola. Kirk (1984) maintains both Blakeslea and Choanephora as valid genera, not because of the number of spores in the sporangiolum but because of the presence of a longitidinal suture in the sporangiolar wall of Blakeslea spp. and the absence of such a suture in the sporangiola wall of Choanephora spp. The sporangiolar wall separates readily from the spore wall in species of Blakeslea; this is not true in species of Choanephora.
Several monographic treatments other than the one by Kirk (1984) have been published on the Choanephoraceae including those by Hesseltine (1953), Hesseltine and Benjamin (1957), Mehrotra and Mehrotra (1964), Cheng and Wu (1964), and Mil’ko and Beljakova (1970).
Blakeslea trispora has been used extensively to study the sexual hormone system (ß-carotene to trisporic acids) in the Mucorales (Burmester et al., 2007; Schachtschabel et al., 2008). The aforementioned species (B. trispora) also is used to convert ß-carotene to carotene compounds that are useful in industry using single strains or mated cultures of this fungus (Böhme et al. 2006; Kuzina and Cerdá-Olmeda, 2006, 2007). The biology of heterothallism and its use in biotechnology has been discussed by Feofilova (2006). The genes involved in sexuality and carotene synthesis have been studied (Kuzina et al., 2008).
Some taxa are weakly parasitic on certain flowering plants in nature (Choanephora spp.) or they cause storage rots [Gilbertella persicaria (E.D. Eddy) Hesselt.] and can be isolated from infected hosts (Wolf, 1917; Kucharek and Simone, 1983; Ginting et al., 1996; Sakai et al., 2000; Papp et al., 2001). The fungi also can be isolated from soil and dung.
Choanephoraceae Schröter 1893 [In Engler and Prantl, Die natürl. Pflanzenfam. 1(1): 131](Kirk, 1984-monograph and key to genera).
= Gilbertellaceae Benny, 1991 (Mycologia 83: 151) fide Voigt and Olsson (2008).
Sporophores arising directly from the substrate mycelium or aerial hyphae, simple or branched, producing either sporangia or sporangiola, never both. Sporangia large, multispored, and columellate, or smaller, few-spored, and acolumellate, wall persistent, echinulate, with one or more weak longitudinal lines of rupture; sporangiospores with long, hyaline, polar appendages, and a hyaline, smooth wall or a brown, longitudinally, striate wall. Sporangiola uni- or multispored, wall persistent, of two types: 1) wall entire, appears inseparable from spore wall; sporangiospores without appendages, brown, smooth or more or less longitudinally striate; 2) wall ruptures longitudinally and separates from the spore wall; sporangiospores with hyaline, polar appendages, and a brown, striate wall. Zygospores with a thin, hyaline, relatively smooth zygosporangial wall and a zygospore wall that is thicker, brown, and striate, suspensors apposed, often entwined, without appendages, or the zygosporangial wall is relatively thick, pigmented and ornamented and the zygospore wall is thick, hyaline, and smooth with opposed, nonappendaged suspensors
Type genus: Choanephora Currey.
KEY TO THE GENERA OF CHOANEPHORACEAE
A. Only relatively large, columellate sporangia produced —— B
AA. Sporangiola always present, may be accompanied by sporangia —— C
B. Causing a hard rot of fruits including nectarines, peaches and tomatoes and can be isolated from soil; grows and sporulates well in culture on most fungal culture media; zygospores formed on opposed suspensors (Mucor-type zygospores) in the lower aerial hyphae —— Gilbertella
BB. Usually isolated only from soil; sporulation only occurs on a few nutrient-poor fungal culture media; zygospores with apposed, entwined suspensors that are tongs-like (Choanephora-type zygospores) —— Poitrasia
C. Sporangiolar wall separable, with longitudinal line or lines of weakness —— Blakeslea
CC. Sporangiolar wall not separable, without longitudinal lines of weakness —— Choanephora
Synopsis of Genera
Blakeslea Thaxter, 1914 [Bot. Gaz. (Crawfordsville) 58: 353]; 2 spp. (Thaxter, 1914—ILLUS.; Mehrotra and Baijal, 1968—illus.; Benny and O’Donnell, 1978—illus.; Mikawa, 1979—illus. as Choanephora trispora (Thaxt.) Sinha; Kirk, 1984—ILLUS. and KEY TO SPP.; Zheng and Chen, 1986-illus.; Ho and Chang, 2003—illus.).
Choanephora Currey, 1873 (J. Linn. Soc., Bot. 13: 578); 2 spp. (Thaxter, 1903—ILLUS.; Hesseltine, 1953—illus. and key to spp.; Poitras, 1955—illus.; Hesseltine and Benjamin, 1957—illus.; Mehrotra and Mehrotra, 1964—illus. and key to spp.; Cheng and Wu, 1964—illus. and key to spp.; Mil’ko and Beljakova, 1970—illus. and key to spp.; Kirk, 1984—ILLUS. and KEY TO SPP.).
? = Cunninghamia Currey, 1873 [J. Linn. Soc., Bot. 13: 334; non Cunninghamia R. Br., 1826 (In Richard, Comm. Bot. Conif. Cycad, p. 149)].
? = Choanephorella Vuill., 1904 (Bull. Soc. Mycol. France 20: 28; nomen nudum, Art. 41.1 of the ICBN (McNeill et al., 2006).
Gilbertella Hesseltine, 1960 (Bull. Torrey Bot. Club 87: 24); 1 sp. (Eddy, 1925-illus.; Hesseltine, 1960—illus.; Mehrotra and Mehrotra, 1963—illus.; Mehrotra, 1963a, 1963b, 1966; Cheng and Hu, 1965—illus.; Sarbhoy, 1966a—illus., 1966b—illus.; O’Donnell et al., 1977a—illus., 1977b—illus.; O’Donnell and Benny, 1978-illus.; Benny, 1991—ILLUS.).
Poitrasia Kirk, 1984 (Mycol. Papers 152: 51); 1 sp. (Naganishi and Kawakami, 1955—illus. as Blakeslea circinans Naganishi & Kawakami; Hesseltine and Benjamin, 1957—illus. as Choanephora circinans (Nag. & Kawak.) Hesseltine & C. R. Benjamin; Kirk, 1977—illus.; Mikawa, 1979—illus.; Kirk, 1984—ILLUS.).
Genera Not Accepted Here but Included in Choanephoraceae by Some Authors
[Mycotypha, see Mycotyphaceae (Mucorales)].
[Cunninghamella, see Cunninghamellaceae (Mucorales)].
[Radiomyces, see Radiomycetaceae (Mucorales)].
[Rhopalomyces, see Helicocephalidaceae (Zoopagales)].
[Sigmoideomyces, see Sigmoideomycetaceae (Zoopagales)].
[Thamnocephalis, see Sigmoideomycetaceae (Zoopagales)].
Bibliography
Benjamin, R.K. 1959. The merosporangiferous Mucorales. Aliso 4: 321-433.
Benjamin, R.K. 1979. Zygomycetes and their spores, pp. 573-616. In: B. Kendrick (Ed.). The whole fungus: the sexual-asexual synthesis. Vol. 2. National Museums of Canada, Ottawa, Canada.
Benny, G.L. 1991. Gilbertellaceae, a new family of the Mucorales (Zygomycetes). Mycologia 83:150-157.
Benny, G.L., and K.L. O’Donnell. 1978. Choanephora trispora, pp. 135-136. In: M.S. Fuller (ed.). Lower fungi in the laboratory. Palfrey Contributions in Botany. No. 1. Department of Botany, University of Georgia, Athens, Georgia.
Böhme, K., C. Richter, and R. Pätz. 2006. New insights into mechanisms of growth and ß-carotene production in Blakeslea trispora. Biotechnology 1:1080-1084.
Burmester, A., M. Richter, K. Schultze, K. Voelz, D. Schachtschabel, W. Boland, J. Wöstemeyer and C. Schimek. 2007. Cleavage of ß-carotene as the first step in sexual hormone synthesis in Zygomycetes is mediated by a trisporic acid regulated ß-carotene oxygenase. Fungal Genetics and Biology 44: 1096-1108.
Cannon, P.F., and P.M. Kirk. 2007. Fungal families of the World. Wallingford, United Kingdom, CAB International. 456 p.
Cheng, J.-y., and F.-m. Wu. 1964. The Mucorales of China. I. Choanephoraceae. Acta Phytotaxonomica Sinica 9:13-30.
Cheng, J-y., and F.-m. Hu. 1965. A new species of Gilbertella. Acta Phytotaxonomica Sinica 10:105-109.
Eddy, E.D. 1925. A storage rot of peaches caused by a new species of Choanephora. Phytopathology 15:607-610.
Feofilova, E.P. 2006. Heterothallism of mucoraceous Fungi: a review of biological implications and uses in biotechnology. Applied Biochemistry and Microbiology 42: 439-454.
Ginting, G., E.I. Zehr and S.W. Westcott III. 1996. Inoculum sources and characterization of isolates of Gilbertella persicaria from peach fruit in South Carolina. Plant Disease 80: 1129-1134.
Hesseltine, C.W. 1953. A revision of the Choanephoraceae. Amer. Midl. Nat. 50: 248-256.
Hesseltine, C.W. 1955. Genera of Mucorales with notes on their synonymy. Mycologia 47:344-363.
Hesseltine, C.W. 1960. Gilbertella gen. nov. (Mucorales). Bull. Torrey Bot. Club. 87:21-30.
Hesseltine, C.W., and C.R. Benjamin. 1957. Notes on the Choanephoraceae. Mycologia 49:723-733.
Hesseltine, C.W., and J.J. Ellis. 1973. Mucorales, pp. 187-217. In: G.C. Ainsworth, F.K. Sparrow and A.S. Sussman. [eds.]. The Fungi. Vol. 4b. Academic Press, New York. U.S.A.
Ho, H.-M., and L.-L. Chang. 2003. Notes on Zygomycetes of Taiwan (III). Two Blakeslea species new to Taiwan. Taiwania 48:232-238.
Kirk, P.M. 1977. Scanning electron microscopy of zygospore formation in Choanephora circinans (Mucorales). Trans. Brit. Mycol. Soc. 68:429-434.
Kirk, P.M. 1984. A monograph of the Choanephoraceae. Mycol. Paper 152:1-61.
Kirk, P.M., P.F. Cannon, D.W. Minter, and J.A. Stalpers. 2008. Ainsworth & Bisby’s Dictionary of the Fungi. 10th Ed. Wallingford, United Kingdom, CAB International. 771 p.
Kucharek, T., and G. Simone. 1983. Wet rot of vegetable crops. University of Florida, Gainesville. PP 11:1-2.
Kuzina, V., and E. Cerdá-Olmeda. 2006. Modification of sexual development and coarotene production by acetate and other small carboxylic acids in Blakeslea trispora and Phycomyces blakesleeanus. Applied and Environmental Microbiology 72:4917-4922.
Kuzina, V., and E. Cerdá-Olmeda. 2007. Ubiquinone and ß-carotene production in the Mucorales Blakeslea and Phycomyces. Appl. Microbiol. Biotechnol. 76:991-999.
Kuzina, V., H. RamÃrez-Medina H. Vissar, A.J.J. van Ooyen, E. Cerdá-Olmeda, and J.A. van den Berg. 2008. Genes involved in carotene synthesis and mating in Blakeslea trispora. Current Genetics 54:143-152.
Lendner, A. 1908. Les Mucorinées de la Suisse. Beiträge zur Kryptogamenflora der Schweiz. III. K.-J. Wyss, Bern, Switzerland. 180 p.
Mehrotra, B.S., and U. Baijal. 1968. Is Blakeslea a valid genus? J. Elisha Mitchell Sci. Soc. 84:207-210.
Mehrotra, B.S. and M.D. Mehrotra. 1963. A morphological and physiological study of Gilbertella in India. Mycologia 55:582-594.
Mehrotra, B.S., and M.D. Mehrotra. 1964. Taxonomic studies of Choanephoraceae in India. Mycopath. Mycol. Appl. 22:21-39.0
Mehrotra, M.D. 1963a [1964]. Fruit rot of pear caused by Gilbertella persicaria var. indica. Sydowia 17:124-125.
Mehrotra, M.D. 1963b [1964]. Fruit rot of tomato caused by Gilbertella persicaria. Sydowia 17:17-19.
Mehrotra, M.D. 1966. Fruit rot of peach by Gilbertella persicaria var. indica from India. Mycopath. Mycol. Appl. 29:151-154.
Mikawa, T. 1979. A taxonomic study on Japanese sporangiferous Mucorales (6). J. Japan. Bot. 54:289-300.
McNeill, J., F.R. Barrie, H.M. Burdet, V. Demoulin, D.L. Hawksworth, K. Marhold, D.H. Nicolson, J. Prado, P.C. Silva, J.E. Skog, J.H. Wiersema, and N.J. Turland. [eds.]. 2006. International Code of Botanical Nomenclature (Vienna Code). [Regnum Vegetabile Vol. 126]. A.R.G. Gantner Verlag KG, Ruggell, Liechtenstein. 568 p.
Mil’ko, A.A. 1974. Opredeltiel’ mukoral’nykh gribov Key to the identification of Mucorales. ‘Naukova Dumka’ , Kiev, Ukraine. 303 p.
Mil’ko, A.A., and L.A. Beljakova. 1970. The genus Choanephora Currey (Mucorales). Mikrobiologiya 38:894-902 [English translation available in Mikrobiologiya 38:864-770])
Naganishi, H., and H. Kawakami. 1955. On Blakeslea Thaxter in Japan. (II) Bl. circinans sp. nov. Bull. Fac. Engineer., Hiroshima Univ. 4:183-187.
O’Donnell, K.L., and G.L. Benny. 1978. Gilbertella persicaria, pp. 123-124. In: M.S. Fuller (Ed.). Lower fungi in the laboratory. Palfrey Contributions in Botany. No. 1. Department of Botany, University of Georgia, Athens, Georgia.
O’Donnell, K.L., J.J. Ellis, C.W. Hesseltine, and G.R. Hooper. 1977a. Morphogenesis of azygospores in Gilbertella persicaria (+) by imperfect hybridization with Rhizopus stolonifer (-). Can . J. Bot. 55:2721-2727.
O’Donnell, K.L., J.J. Ellis, C.W. Hesseltine, and G.R. Hooper. 1977b. Zygosporogensis in Gilbertella persicaria. Can. J. Bot. 55:662-675.
Papp, T., M. Vastag, T.J. Michailides, L. Ferenczy, and C. Vágvölgyi. 2001. Genetic variability of the postharvest pathogen Gilbertella persicaria: identification of randomly amplified polymorphic DNA (RAPD) markers correlating with (+) and (-) mating types. Antonie Van Leeuwenhoek 80: 301-309.
Papp, T., K. Acs, I. Nyilasi, E. Nagy, and C. Vágvölgyi. 2003. Phylogenetic relationship of the genus Gilbertella and related genera within the order Mucorales based on 5.8 S ribosomal DNA sequences. Acta Bot. Hung. 54:393-402.
Pidoplichko, N.M., and A.A. Mil’ko. 1971. Atlas mukoral’vykh gribov Atlas of the Mucorales. Izdat. ‘Naukova Dumka,’ Kiev, Ukraine. 115p.
Poitras, A.W. 1955. Observations on asexual and sexual reproductive structures of the Choanephoraceae. Mycologia 47:702-713.
Sakai, S., M. Kato, and H. Nagamasu. 2000. Artocarpus (Moraceae)-gall midge pollination mutualism mediated by a male-flower parasitic fungus. Am. J. Bot. 87:440-445.
Sarbhoy, A.K. 1966a. Gilbertella persicaria. C.M.I. Descriptions of pathogenic fungi and bacteria no. 104:1-2.
Sarbhoy, A.K. 1966b. Gilbertella persicaria var. indica. C.M.I. Descriptions of pathogenic fungi and bacteria no. 105:1-2.
Schachtschabel, D., A. David, K.—D. Menzel, C. Schimek, J. Wöstemeyer, and W. Boland. 2008. Cooperative biosynthesis of trisporoids by the (+) and (—) mating types of the zygomycete Blakeslea trispora. ChemBioChem 9:3004-3012.
Schröter, J. 1893. Mucorineae, pp. 119-134. In A. Engler and K. Prantl, Die natürlichen Pflanzenfamilien. I Teil, 1. Abth. Wilhelm Engelmann, Leipzig.
Thaxter, R. 1903. Mycological notes, 1-2. Rhodora 5:97-108.
Thaxter, R. 1914. New or peculiar Zygomycetes. 3: Blakeslea, Dissophora and Haplosporangium, nova genera. Bot. Gaz. (Crawfordsville) 58:353-366.
Voigt, K., and I. Olsson. 2008. Molecular phylogenetic and scanning electron microscopical analysis places the Choanephoraceae and the Gilbertellaceae in a monophyletic group within the Mucorales (Zygomycetes, Fungi). Acta Biologica Hungarica 59: 365-383.
Wolf, F.A. 1917. A squash disease caused by Choanephora cucurbitarum. Journal of Agricultural Research 8:319-329.
Zheng, R.-y., and G.-q. Chen. 1986. Blakeslea sinensis sp. nov., a further proof for retaining the genus Blakeslea. Acta Mycol. Sinica Suppl. 1:40-55.
Zycha, H., R. Siepmann, and G. Linnemann. 1969. Mucorales eine Beschreibung aller Gattungen und Arten dieser Pilzgruppe. Lehre, J. Cramer. 355 p
Updated Jun 01, 2010