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Heterothallism of Mucoraceous Fungi: a Review of Biological Implications and Uses in Biotechnology E

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Heterothallism of Mucoraceous Fungi: a Review of Biological Implications and Uses in Biotechnology E ISSN 0003-6838, Applied Biochemistry and Microbiology, 2006, Vol. 42, No. 5, pp. 439–454. © MAIK “Nauka/Interperiodica” (Russia), 2006. Original Russian Text © E.P. Feofilova, 2006, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2006, Vol. 42, No. 5, pp. 501–519. Heterothallism of Mucoraceous Fungi: A Review of Biological Implications and Uses in Biotechnology E. P. Feofilova Winogradsky Institute of Microbiology, Russian Academy of Sciences, Moscow, 117811 Russia e-mail: feofi[email protected] Received October 25, 2005 Abstract—The phenomenon of heterothallism in filamentous fungi is reviewed, with emphasis on the discus- sion 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 communi- cation 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 phenom- enon of heterothallism. Specifically, it may be used to obtain a series of isoprenoid compounds, such as β-car- otene and lycopene (which exhibit pronounced antioxidant activity), as well as sterols and trisporic acids. DOI: 10.1134/S0003683806050012 Microbial populations have been considered THE ESSENCE OF THE TERM recently not as separately developing cells but as a com- HETEROTHALLISM AND ITS PREVALENCE munity with a close communication between individual AMONG FUNGI cells [1, 2]. The cells communicate due to the evolu- The reproduction of the majority of fungi displays tionary emergence of the corresponding mechanisms an interesting specific feature. In 1904, Blakeslee [7] allowing signals from external space to be perceived studied the sexual reproduction of mucoraceous fungi, and transformed [3]. These signals are mainly chemical in particular, Blakeslea trispora, and found that zygotes compounds and allow the cell to adapt quickly to exter- were not formed when these fungi were grown from one spore. The main condition for sexual process is nal impacts by changing its chemical composition. In copulation of the mycelia different with respect to sex. turn, the adapted cells generate new chemical com- Blakeslee named these mycelia (+) and (–), and the pounds (new signals), whose synthesis is determined phenomenon itself got the name heterothallism. Some- by the stress effect. what later, heterothallism was discovered in other Muc- orales, for example, the fungi of the genus Absidia. The We still know little about the chemical “language” study demonstrated that these fungi differed in the size used by the cells to communicate. The communication and structure of their copulative organs; thus, in this of heterothallic fungal strains during sexual reproduc- case, the (+) and (–) designations of mycelia may be tion, when the cells interact via specific molecules replaced with female and male mycelia, and the term called hormones, is most studied in this respect [4–6]. heterothallism acquires the meaning of occurrence of The phenomenon of heterothallism, connected with the different sexes; correspondingly, homothallism is most important cellular process—sexual reproduction, regarded as hermaphrodism [8]. whose individual stages are controlled by special hor- Heterothallism, first discovered in Mucorales, is mones involved in the interactions between sexual part- now found in virtually all fungal groups; however, it is ners—is the best illustration of the need to study inter- prevalent and studied best for mucoraceous fungi. About 60 species of the last group are heterothallic and cellular interactions. Consideration of the heterothal- only 20 are homothallic [8]. Heterothallism is also lism in filamentous fungi from this particular widespread in Neomycota in the class Basidiomycetes. standpoint enables a deeper understanding of this Overall, 50 species of Ustilaginaceae display this phe- unique phenomenon and makes it possible to draw an nomenon; of the studied Hymenomycetes species, over analogy with multicellular eukaryotes. 50 are heterothallic. 439 440 FEOFILOVA Heterothallism is also spread among the organisms and at particular stages of the organism’s development, that were previously ascribed to fungi, namely, hindering determination of their chemical nature. In oomycetes (now the kingdom Chromista). Of lower addition, fungal hormones can perform additional func- eukaryotes, heterothallism is met in marine alga; for tions in the cell metabolism, another factor that makes example, brown alga (genus Fucus) have motile male their identification difficult. For example, the sex hor- gametes and nonmotile eggs, while the genera Ectocar- mone of mucoraceous fungi—trisporic acids (TSA)— pus and Cutleris have motile male and female gametes was first discovered as stimulators of carotenogenesis. [9]. The sexual process of the ciliate (protozoon) Ble- Similar to other organisms, the most essential pro- pharisma intermedia involves two types of cells, type 1 cess for fungi in preserving the species is sexual repro- and type 2. duction, and nature in this case spent much trouble to The heterothallic cells differ according to the mating make this process reproducible, using for this purpose types. The fungi have bipolar and tetrapolar mating regulation with hormones. Due to the specific chemical types [11]. The former is characteristic of Zygomycetes structure, it is hormones that are able to control the but is also found in Ascomycetes and Basidiomycetes. reproduction of heterosexual organisms. It is appropri- In the last group, bipolar mating was discovered in ate to dwell here on the example of fungal hormones, Ustilago gordei. The tetrapolar mating is characteristic the majority of which are lipid-like compounds or, of Basidiomycetes, studied best for Coprinus cenereus more precisely, terpenoids [5]. These molecules are and Schizophyllum commune, and found in several now regarded as evolutionarily the most ancient com- U. maidis species. Zygomycetes have a true bipolar pounds that display “the effect of small molecules” (the mating of (+) and (–) mycelia, which differ sexually theory of dynamic play of small molecules in evolu- according to their ability to synthesize sex hormones tion) [14]. Presumably, it is not accidental that the hor- (see below). However, there is another way of provid- mones of fungi and pseudofungi involved in the sexual ing copulation between different species—the so-called process are terpenes or sterols. For example, the female lecherous mating. This mating type was discovered in sex hormone of the water fungus Achlia ambisexua- the parasitic fungi Parasitella, growing on Absidia, lis—antheridiol (previously called hormone A)—is a which is the host. In this case, the parasite can play the steroid C29H42O5) causing hyphal branching. The male role of the opposite-sign copulating strain, and pseu- cells in turn synthesize hormone B (oogoniol), which is dosexual structures are formed [12]. The bipolar mat- a sterol ester (C H O ), inducing the female cell to ing system of certain Ascomycetes is called ideomor- 33 54 6 develop oogonia. Hormone B is 7-keto-ë29-sterol lack- phic. This term means the sequence of the loci of cop- ing a lactone ring, characteristic of antheridiol. The ste- ulating species that do not display the homology to the rol fucosterol is the precursor of both hormones. copulating strain of the opposite sex. This system is characteristic of Neurospora crassa and several other Sterols are also involved in the reproduction of Ascomycetes [12]. pseudofungi. Pseudofungi (Phytophthora and Pythium) are incapable of synthesizing sterols and grow well in the absence of these compounds; however, they require HORMONE-LIKE COMPOUNDS ARE sterols for reproduction. For example, ergosterol stim- THE CHEMICAL LANGUAGE OF SEXUAL ulates Phymatotrichum omnivorum to develop conidia REPRODUCTION OF HETEROTHALLIC FUNGI and Phythophtora sp. to develop sporangia. Sterols are The sexual reproduction of fungi is controlled by also necessary for the sexual reproduction (oospore for- special compounds called hormones. This term was mation) of P. coctorum. ë29 The most active in these α first defined in 1935 for plants [4] and later supple- processes are ë27 sterols with an -configuration at C24 mented with reference to fungi [6]. Thus, hormones are of the side chain—sistosterols and stigmasterols. ë27 compounds whose function is the regulation of sexual sterols are less active, and ë28 sterols display an inter- process. The fungal hormones are classified according mediate activity. Cholesterol stimulates heterothallic to their specific properties into pheromones, growth strains of Phytophthora to form oospores, and this substances, morphogens, and sex factors by analogy effect is more pronounced when cholesterol is applied with sex
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