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Insights from Aspergillus Species Paul S REVIEW ARTICLE Sexual development and cryptic sexuality in fungi: insights from Aspergillus species Paul S. Dyer & Ce´ line M. O’Gorman School of Biology, University of Nottingham, Nottingham, UK Downloaded from https://academic.oup.com/femsre/article/36/1/165/534783 by guest on 24 September 2021 Correspondence: Paul S. Dyer, School of Abstract Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK. Tel.: Major insights into sexual development and cryptic sexuality within filamen- +44 115 9513251; fax: +44 115 9513251; tous fungi have been gained from investigations using Aspergillus species. Here, e-mail: [email protected] an overview is first given into sexual morphogenesis in the aspergilli, describing the different types of sexual structures formed and how their production is Received 12 May 2011; accepted 4 influenced by a variety of environmental and nutritional factors. It is argued September 2011. Final version published that the formation of cleistothecia and accessory tissues, such as Hu¨lle cells online 6 October 2011. and sclerotia, should be viewed as two independent but co-ordinated develop- DOI: 10.1111/j.1574-6976.2011.00308.x mental pathways. Next, a comprehensive survey of over 75 genes associated with sexual reproduction in the aspergilli is presented, including genes relating Editor: Gerhard Braus to mating and the development of cleistothecia, sclerotia and ascospores. Most of these genes have been identified from studies involving the homothallic Keywords Aspergillus nidulans, but an increasing number of studies have now in addition cleistothecia; sclerotia; mating type; characterized ‘sex-related’ genes from the heterothallic species Aspergillus Petromyces; sexual morphogenesis; fumigatus and Aspergillus flavus. A schematic developmental genetic network is asexuality. proposed showing the inter-relatedness between these genes. Finally, the dis- covery of sexual reproduction in certain Aspergillus species that were formerly considered to be strictly asexual is reviewed, and the importance of these find- ings for cryptic sexuality in the aspergilli as a whole is discussed. The genus Aspergillus comprises approximately 250 Introduction species (Samson & Varga, 2010) that are collectively ‘Sexuality in fungi has long been recognized as one of the termed the ‘aspergilli’. It should be noted that this num- more perplexing yet intriguing facets of the biology of ber is probably an underestimation, and conflicting this large and varied group of micro-organisms’ (Raper, reports exist on the actual number of accepted species 1966). Despite a further 40 years of research since John owing to the complex taxonomy of the genus (Peterson, Raper wrote this statement in his book Genetics of Sexual- 2008). Aspergillus species have traditionally been recog- ity in Higher Fungi, the process of sexual reproduction in nized by the presence of a common morphological fea- fungi is still perplexing mycologists. However, insights ture, the ‘aspergillum’, an asexual reproductive structure have been gained into many aspects of fungal sexuality consisting of a characteristic conidiophore culminating in following the application of modern molecular genetic an expanded bulbous region on which is borne phialides techniques. For example, genes involved in the determi- and metullae that generate chains of conidia (Bennett, nation of breeding systems have been identified together 2009). Phylogenetic analysis has shown that they are with a repertoire of genes involved in sexual develop- essentially a monophyletic group (Peterson, 2008). They ment, and such ‘sex-related’ genes have been used to have a ubiquitous distribution, being present in decaying MICROBIOLOGY REVIEWS MICROBIOLOGY investigate the genetic basis of sexuality and asexuality in vegetation, soils and dust worldwide (Klich, 2002b; Ben- fungi. Many of these advances have come through or nett, 2010). The aspergilli are of particular importance have been aided by the study of Aspergillus species, which because they include in their number species that are will form the focus of the present review. highly beneficial to mankind, but others that are highly FEMS Microbiol Rev 36 (2012) 165–192 ª 2011 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved 166 P.S. Dyer & C.M. O’Gorman detrimental. Thus, certain species are used in food pro- Table 1. Teleomorphic genera with known Aspergillus anamorphs duction, in industry for metabolite production including Number of Homothallic : as a source of drugs, and as laboratory model organisms Genus species* Examples heterothallic for basic and applied research. By contrast, other Aspergil- Chaetosartorya 3 C. chrysella, 3:0 lus species can cause contamination of food stocks and C. cremea give rise to life-threatening infections in immunocompro- Dichotomomyces 2 D. albu, D. cejpii 2:0 mised hosts (Bennett, 2009, 2010). Emericella 43 E. nidulans, 42 : 1 The aspergilli have proved especially valuable in studies E. heterothallica of fungal sexuality because they include species with a Eurotium 64 E. herbariorum, 64 : 0 range of different reproductive modes. Some ‘mitosporic’ E. chevalieri Fennellia 3 F. flavipes, F. nivea 3:0 species are only known to reproduce by asexual means Downloaded from https://academic.oup.com/femsre/article/36/1/165/534783 by guest on 24 September 2021 Neocarpenteles 1 N. acanthosporum 1:0 and have been traditionally classified in the fungal phylum Neopetromyces 1 N. muricatus 1:0 the Deuteromycota, which encompasses fungi lacking a Neosartorya 40 (46)† N. fischeri, 33 : 7 known sexual state (Taylor et al., 1999). By contrast, ‘mei- N. fumigata osporic’ species can also reproduce by sexual means and Penicilliopsis 2 P. dybowskii, 2:0 so have been traditionally classified in the fungal phylum P. flavidus the Ascomycota, whose characteristic feature is sexual Petromyces 5 P. alliaceus, 1:4 P. flavus reproduction involving the production of ascospores Sclerocleista 2 S. ornata, 2:0 within asci. In the case of meiosporic Aspergillus species, S. thaxteri they exhibit either heterothallic (obligate outbreeding) or Warcupiella 1 W. spinulosa 1:0 homothallic (self-fertile) sexual breeding systems. The *All legitimate species registered at MycoBank (www.mycobank.org) division of Aspergillus species into either the Deuteromy- on 5 May 2011. Note that the number of Aspergillus species regis- cotina or the Ascomycotina is arguably misleading because tered at MycoBank is higher than the figure reported by Samson & phylogenetic analysis shows that they form a united group Varga (2010). (Peterson, 2008), and the term ‘Deuteromycotina’ has †The number in parentheses includes six unconfirmed species pro- now largely been replaced by the mitosporic or meiosporic posed by Peterson (2008). terminology (Ku¨ck & Po¨ggeler, 2009). The majority of accepted Aspergillus species (approximately two-thirds of Overview of sexual development in the taxa) are only known to reproduce by asexual means, aspergilli whilst those that do exhibit sexual cycles are overwhelm- ingly homothallic in nature with few heterothallic species Morphology of teleomorph states described (Table 1) (Dyer, 2007; Kwon-Chung & Sugui, 2009). Elucidating the genetic basis of such differences in The Pezizomycotina encompasses those Ascomycota that reproductive mode is proving a fascinating challenge. grow by production of filamentous hyphae. In this sub- There have been a number of dedicated reviews over phylum, sexual spores (ascospores) are housed in one of the past decade dealing with different aspects of sexual four main types of fruiting body (ascomata/ascocarps): reproduction in Aspergillus species, some reviewing the cleistothecia, perithecia, apothecia or pseudothecia. They aspergilli in general (e.g. Dyer, 2007; Geiser, 2008) whilst differ in their size, shape, style and organization of the others have focussed specifically on Aspergillus nidulans asci, and presence and type of interascal sterile hyphae (e.g. Braus et al., 2002; Han et al., 2008a; Han, 2009; Han (Po¨ggeler et al., 2006). Members of the genus Aspergillus & Han, 2010). The present review will first give an over- produce their ascospores in cleistothecia, which are the view of sexual reproduction in the aspergilli as a whole only ascomatal type that fully encloses the asci and and then provide a summary of the current state of ascospores (Gre. kleistos, closed + Gre. the¯kion, small knowledge of genes involved with sexual development in case). Cleistothecia may contain up to 100 000 asci, each Aspergillus species. This includes updating information enclosing (with very rare exceptions) eight ascospores; in from previous reviews and covering new material relating the case of A. nidulans, an average cleistothecium may to recently characterized genes, and the involvement of contain around 80 000 viable ascospores (Pontecorvo, sex-related genes in sclerotial development. Finally it will 1953; Braus et al., 2002). Rather than being forcefully dis- describe the recent discoveries of sexual cycles in Aspergil- charged, ascospores are released following the natural lus fumigatus, Aspergillus flavus, Aspergillus parasiticus and breakdown of the ascus wall and the outer wall (perid- Aspergillus nomius and discuss the significance of these ium) of the cleistothecium in their natural environment findings in terms of cryptic sexuality in the aspergilli such as soil or decaying vegetation. One exception is given their economic and medical importance.
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