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Nematode-Trapping Fungi

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Nematode-Trapping Fungi Current Research in Environmental & Applied Mycology Nematode-Trapping Fungi Swe A1, Li J2, Zhang KQ2, Pointing SB1, Jeewon R1 and Hyde KD3* 1School of Biological Science, University of Hong Kong, Pokfulam Hong Kong 2Laboratory for Conservation and Utilization of Bio-resources, and Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming, P. R. China 3School of Science, Mae Fah Luang University, Chiang Rai, Thailand Swe A, Li J, Zhang KQ, Pointing SB, Jeewon R, Hyde KD. 2011 – Nematode-Trapping Fungi. Current Research in Environmental & Applied Mycology 1(1), 1–26. This manuscript provides an account of nematode-trapping fungi including their taxonomy, phylogeny and evolution. There are four broad groups of nematophagous fungi categorized based on their mechanisms of attacking nematodes. These include 1) nematode-trapping fungi using adhesive or mechanical hyphal traps, 2) endoparasitic fungi using their spores, 3) egg parasitic fungi invading nematode eggs or females with their hyphal tips, and 4) toxin-producing fungi immobilizing nematodes before invasion The account briefly mentions fossil nematode-trapping fungi and looks at biodiversity, ecology and geographical distribution including factors affecting their distribution such as salinity. Nematode-trapping fungi occur in terrestrial, freshwater and marine habitats, but rarely occur in extreme environments. Fungal-nematodes interactions are discussed the potential role of nematode-trapping fungi in biological control is briefly reviewed. Although the potential for use of nematode-trapping fungi is high there have been few successes resulting in commercial products. Key words – Ascomycetes – Biocontrol – Biodiversity – Fossil fungi – Fungi – Nematodes – Phylogeny Article Received 4 June 2011 Accepted 6 June 2011 Published online 25 June 2011 *Corresponding author: Kevin D. Hyde – e-mail – [email protected] Table of contents Introduction 2 Taxonomy, phylogeny and evolution of nematode-trapping fungi 2 Background of generic classification 2 Phylogenetic significance and evolution of trapping devices 4 Ancient nematode-trapping fungi 4 Biodiversity of nematode-trapping fungi 4 Ecology, occurrence and geographical distribution 6 Factors affecting the distribution of NTF 6 Effect of salinity 7 Ecological speciation 7 Fungal-nematode interactions 8 Host recognition, adhesion, host specificity and infection process 8 1 Extracellular enzymes involved in nematode infestation process 10 Biological control of nematodes 10 Use of NTF to control animal gut nematodes 11 Use of NTF in traditional or natural biocontrol of plant nematodes 11 Using advance techniques 11 Commercialization of products 12 Introduction amongst mycologists. Many generic names There are four broad groups of nemato- have been given to nematode-trapping fungi phagous fungi categorized based on their but the basis on which species were circumscri- mechanisms of attacking nematodes (Liu et al. bed to different genera was unclear and sub- 2009). These include (1) nematode-trapping jective. Since 1930, nematode-trapping fungal fungi using adhesive or mechanical hyphal have been described and classified mostly in traps, (2) endoparasitic fungi using their spores, Arthrobotrys Corda, Dactylaria Sacc, and Dac- (3) egg parasitic fungi invading nematode eggs tylella Grove. or females with their hyphal tips, and (4) toxin- Corda (1839) established the genus Ar- producing fungi immobilizing nematodes throbotrys with A. superba Corda as the type before invasion (Kendrick et al. 2001, Liu et al. species. Characteristics of this genus are hya- 2009). line conidiophores which produce conidia The first nematode-trapping fungus to be asynchronously on short denticles at swollen described was Arthrobotrys oligospora Fresen. conidiogenous heads or clusters of pronounced in 1852, but at that time its predatory habit was denticles (De Hoog 1985). Conidia are subhya- unknown. The predatory habit was first obser- line, obovoidal or clavate and (0–)1(–6)-sep- ved 36 years later by Zopf (1888). Since nema- tate. Trapping devices are constricting rings, tode-trapping fungi have considerable potential adhesive nets, hyphae or adhesive knobs (De for biological control of nematodes, there have Hoog 1985). Due to these broad morphological been extensive studies and reviews on their criteria the delimitation from Arthrobotrys is taxonomy, phylogeny, biology, and ecology sometimes problematic, particularly in Dactyl- (Cooke 1963, Kerry 1987, Sayre & Walter ella species which form more than one or two 1991, Sikora 1992, Kerry & Hominick 2002, conidia on each conidiophore (Cooke & Morton et al. 2004, Dong & Zhang 2006, Dickinson 1965). Based on this reason, Van Sikora et al. 2007). In this review, aspects such Oorschot (1985) restricted Dactylella to as taxonomy, phylogeny, diversity, and eco- species with fusiform, multi-septate conidia, logy of nematode-trapping fungi and their while Arthrobotrys species generally have potential in use in biocontrol of nematodes are ovoidal to clavate, 0–3-septate conidia. Van reviewed. Oorschot (1985) recognized 28 species of Ar- throbotrys. Schenck et al. (1977) expanded the Taxonomy, phylogeny and evolution of genus to 47 species. After Schenck et al. (1977) nematode-trapping fungi transferring all predacious species formerly described in Dactylaria to Arthrobotrys, Dacty- Background of the generic classification laria was no longer tenable for nematode- Nematode-trapping fungi are a hetero- trapping species. Recent classification based geneous group of anamorphic ascomycetes mostly on DNA sequence data has resulted in where species are defined primarily based on the transfer of species characterized by adhe- conidial characteristics such as size, septation, sive networks to Arthrobotrys (Scholler et al. and type of conidiogenous cells (Oudemans, 1999). Currently, there are 120 records of 1885, Subramanian, 1963). This has resulted in Arthrobotrys species but this includes basio- considerable ambiguity and confusion in inter- nyms and synonyms (Index Fungorum, 2011). generic classification of these organisms. Since A more realistic estimate is 63 (Kirk et al. the discovery of predacious activity in Arthro- 2008). botrys oligospora (Zopf, 1888), nematode- Monacrosporium was introduced by trapping fungi have attracted much interest Oudemans (1885) with two species, Monacro- 2 Current Research in Environmental & Applied Mycology sporium elegans Oudem. and M. subtile genus in Index Fungorum (Index Fungorum, Oudem. This generic name has been used by 2011). The current names for most species in many authors for several species following the the genus are in Arthrobotrys (1) Dactylella (3) opinion of Oudemans (1885). Subramanian Gamsylella (4) and Monacrosporium (8) and (1964) later selected M. elegans as lectotype only seven species are listed under Dactylellina species for this genus, highlighting the inflated while the remaining are anamorphic Orbilia middle cell of the conidia as the distinguishing (Index Fungorum 2011) generic criterion, and transferred a large num- Drechslerella was described by ber of nematode-trapping fungi from Dacty- Subramanian (1964) based on the type species, lella species to Monacrosporium. Rubner Drechslerella acrochaeta (Drechsler) Subram. (1996) revised most predacious hyphomycetes Scholler et al. (1999) later revised and trans- in Dactylella and Monacrosporium to deli- fered all predacious species forming con- mitate between the two genera. Scholler et al. stricting rings to this genus. Fourteen names (1999), however, proposed a new genus are listed in this genus in Index Fungorum concept for predatory anamorphic Orbiliaceae (Index Fungorum 2011), while Kirk et al. and the genus Monacrosporium was discarded. (2008) estimated there are one species. Species Many nematode-trapping fungal species are Fungorum (2011) currently lists seven names homeless and Monacrosporium is used as their as anamorphic Orbilia, while the other species current name. Currently, 74 taxa are listed in are organized in Arthrobotrys (3), Dactylella Index Fungorum (Index Fungorum, 2011), (1), Geniculifera (1) and Monacrosporium (3). while Kirk et al. (2008) estimate there to be 68 Gamsylella was described by Scholler et species. al. (1999) based on G. arcuata (Scheuer & J. Based on results obtained from morpho- Webster) M. Scholler, Hagedorn & A. Rubner logical and molecular characters, Hagedorn & Scholler et al. (1999) proposed Gamsylella as a Scholler (1999) and Scholler et al (1999) new genus combining all predacious species proposed that nematode-trapping fungi should that formed adhesive columns and unstalked be organized in four genera: Dactylellina M. knob devices to this genus. Li et al. (2005) later Morelet characterized by stalked adhesive transferred those species to Arthrobotrys and knobs including species characterized by non- Yang & Liu (2006) combined this genus with constricting rings and stalked adhesive knobs; Dactylellina based on molecular phylogenetic Gamsylella M. Scholler, Hagedorn & A. analyses. Six taxa belonging to Gamsylella Rubner characterized by adhesive branches and were reported by Index Fungorum (2008) and unstalked knobs; Arthrobotrys characterized by Kirk et al. (2008). Nevertheless, a placement of adhesive networks; and Drechslerella Subram. this genus based on phylogenetic analyses still characterized by constricting rings. Li et al. remains in questioning and therefore it should (2005) emended genus Gamsylella and trans- be revaluated.
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