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Diversity and Evolution of Fusarium Species in the Gibberella Fujikuroi Complex

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Diversity and Evolution of Fusarium Species in the Gibberella Fujikuroi Complex Fungal Diversity Reviews, Critiques and New Technologies Diversity and evolution of Fusarium species in the Gibberella fujikuroi complex Kvas, M.1*, Marasas, W.F.O.1, Wingfield, B.D.2, Wingfield, M.J.1 and Steenkamp, E.T.1,* 1Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI), Faculty of Natural and Agricultural Sciences, University of Pretoria, South Africa 2Department of Genetics, DST/NRF Centre of Excellence in Tree Health Biotechnology (CTHB), Forestry and Agricultural Biotechnology Institute (FABI), Faculty of Natural and Agricultural Sciences, University of Pretoria, South Africa Kvas, M., Marasas, W.F.O., Wingfield, B.D., Wingfield, M.J. and Steenkamp, E.T. (2009). Diversity and evolution of Fusarium species in the Gibberella fujikuroi complex. Fungal Diversity 34: 1-21. The Gibberella fujikuroi complex (GFC) is a monophyletic taxon that includes an assemblage of Fusarium species with similar and overlapping morphological traits that complicates their differentiation. Most of the species in this complex are associated with devastating diseases of many economically important plants. They also produce a remarkably wide range of secondary metabolites or mycotoxins that contaminate food/feed worldwide and can subsequently cause a variety of diseases in humans and animals. Recent developments in molecular systematics have revealed that the Gibberella fujikuroi complex includes at least 50 distinct species or phylogenetic lineages. Of these, 34 species have been formally described using morphological characters, 10 have been also described based on sexual fertility and at least 20 species produce one or more mycotoxins. Here, we review the most important criteria for recognising and defining Fusarium species in the Gibberella fujikuroi complex. We also consider the diversity within this complex, specifically from an evolutionary point of view. We, therefore, discuss the morphological, biological and phylogenetic diversity in the Gibberella fujikuroi complex, by reviewing these properties together with aspects such as mycotoxicology, geographic distribution and host/substrate preference of the various Fusarium species with respect to their phylogeny. Key words: Gibberella fujikuroi species complex, biogeography, host association, mycotoxins, species recognition Article Information Received 3 October 2008 Accepted 20 November 2008 Published online 1 January 2009 *Corresponding authors: Marija Kvas; e-mail: [email protected], Emma T. Steenkamp; e-mail: [email protected] Introduction important vegetable, ornamental and field crops (Kraft et al., 1981; Linderman, 1981; The genus Fusarium represents one of Nelson et al., 1981), while others produce the most important groups of ascomycetous cankers on soft- and hardwood trees fungi. Its members are distributed across the (Bloomberg, 1981; Dwinell et al., 1981, 2001; globe where they are responsible for huge Wingfield et al., 2008). Recently, Fusarium economic losses due to reductions in harvest species have emerged as human pathogens yields and/or the quality of staple foods where they are associated with deeply invasive (Nelson et al., 1983; Leslie and Summerell, infections of immunocompromised patients 2006). At least 80% of all cultivated plants are (Nelson et al., 1994; Nucci and Anaissie, 2002; associated with at least one disease caused by a Summerbell, 2003; Dignani and Anaissie, Fusarium species (Leslie and Summerell, 2004). Fusarium species are further notorious 2006). Various Fusarium species cause de- for producing mycotoxins that contaminate structive diseases on cereal grains (White, food/feed worldwide (reviewed by Marasas et 1980; Parry et al., 1995; Nyvall et al., 1999; al., 1984; Joffe, 1986; Chelkowski, 1989; Goswami and Kistler, 2004), some are respon- Desjardins, 2006), the consumption of which sible for vascular wilts or root rots on many may lead to various serious human and animal 1 diseases, reduced productivity in livestock and and Hansen (1945) argued that the production even death if prolonged exposure occurs of microconidia borne in chains is an unstable (D’Mello et al., 1999; Placinta et al., 1999; character that is inappropriate for reliably Morgavi and Riley, 2007). separating species and varieties in this section. Since its establishment in 1809 by Link, As a result, they lumped together all of the genus Fusarium has received much atten- Wollenweber and Reinking’s species and tion in the scientific literature. A significant recognised only F. moniliforme as a member of portion of these studies dealt with taxonomic Section Liseola. Booth (1971) used the issues (see Leslie and Summerell, 2006), which morphology of conidiogenous cells to separate for the most part have been dominated by the F. moniliforme from its variety F. moniliforme use of morphology to differentiate species and var. subglutinans. In 1983, Nelson and groups or sections. In the nineties, with the colleagues introduced a system that bridged all increased utility of DNA-based methods, it the Fusarium classification systems existing at rapidly became clear that the morphology- that time (Nelson et al., 1983; Leslie and based classifications greatly un-derestimate the Summerell, 2006) and recognised four species true diversity in the genus. The use of DNA (F. anthophilium, F. moniliforme, F. prolifera- sequence information for separating species tum and F. subglutinans) in the Section has, therefore, revolutionised Fusarium taxo- Liseola. They differentiated these based on nomy and it is now widely accepted that taxa shape and production of microconidia in chains previously thought to represent single sections and/or false heads from polyphialides and/or or species are actually species complexes monophialides. Following this system, and the consisting of numerous distinct taxa (e.g. use of some additional morphological traits O’Donnell, 2000; O’Donnell et al., 2000a, (e.g. production of sterile coiled hyphae, 2004). Currently, one of the best-studied pseudochlamydospores), as well as relying on species complexes is the Gibberella fujikuroi molecular and biological traits, various other complex (GFC), which includes numerous Fusarium species in the GFC were mycotoxigenic and/or phytopatho-genic spe- subsequently described (Rheeder et al., 1996; cies. In this paper, we review the taxonomy of Klittich et al., 1997; Nirenberg and O’Donnell, the GFC and its species, as well as the various 1998; Nirenberg et al., 1998; Aoki et al., 2001; criteria used for defining species in the Marasas et al., 2001; Britz et al., 2002b; Zeller complex. We also consider the GFC from an et al., 2003). evolutionary point of view, where we In the 1990s, advances in technology specifically address geographic distribution, have made the use of DNA sequence inform- interacttions with plant hosts and mycotoxin ation more readily accessible for classification pro-duction. purposes and a range of DNA-based methods were then applied to characterise the GFC Taxonomy of the GFC species. These include genomic finger-printing The term “Gibberella fujikuroi complex” techniques such as electrophoretic karyotyping refers to the monophyletic taxon that broadly (Xu et al., 1995), random amplified polymor- corresponds to the Section Liseola, but that phic DNA (RAPD) (Voigt et al., 1995; Viljoen also accommodates certain species originally et al., 1997), polymerase chain reaction (PCR) classified in other Fusarium sections (Fig. 1) restriction fragment length polymorphism (Nirenberg and O’Donnell, 1998; O’Donnell et (RFLP) analysis of specific genes (Steenkamp al., 1998, 2000b; Geiser et al., 2005). Section et al., 1999; Mirete et al., 2003) and amplified Liseola was established by Wollenweber and fragment length poly-morphism (AFLP) Reinking (1935) based on the morphology of analysis (Marasas et al., 2001; Zeller et al., three species (F. moniliforme, F. lactis, F. 2003). For the purposes of direct sequence neoceras) and their varieties that produce analysis, various genomic regions have been macroconidia in sporodochia or pionnotes, evaluated as taxonomic markers (O’Donnell microconidia in false heads and/or chains and and Ciglenik, 1997; O’Donnell et al., 1998, no chlamydospores (Snyder and Hansen, 1945; 2000b; Steenkamp et al., 1999, 2000a; Leslie and Summerell, 2006). Later, Snyder Schweigkofler et al., 2004), including the 2 Fungal Diversity Fig. 1. A maximum likelihood phylogeny of Fusarium species in the GFC (Gibberella fujikuroi complex) based on combined sequence information for the genes encoding translation elongation factor 1 alpha (TEF) and beta-tubulin. All the members of the three well-established clades (O’Donnell et al., 1998, 2000b) are included, with the exception of F. andiyazi as its phylogenetic affinity remains to be determined. Thick branches are supported by bootstrap values >70% as previously reported (O’Donnell et al., 1998, 2000b; Geiser et al., 2005). MP A-J indicates the mating populations in the complex and the tree is rooted with F. oxysporum and F. inflexum. ribosomal RNA (rRNA) internal transcribed translation elongation factor 1-alpha (TEF) has spacer (ITS) widely used for other fungi (Bruns become the marker of choice as it is a single- et al., 1991; Seifert et al., 1995). However, this copy gene that is highly informative among region has been proven ineffective for closely related species (Geiser et al., 2004). classifying Fusarium species, due to the During the course of the last decade, presence of two divergent
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