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Phylogenetics and Evolution of Nematode-Trapping Fungi (Orbiliales) Estimated from Nuclear and Protein Coding Genes

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Phylogenetics and Evolution of Nematode-Trapping Fungi (Orbiliales) Estimated from Nuclear and Protein Coding Genes Mycologia, 97(5), 2005, pp. 1034–1046. # 2005 by The Mycological Society of America, Lawrence, KS 66044-8897 Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes Yan Li their adhesive materials, with their ends meeting to Laboratory for Conservation and Utilization of Bio- form nonconstricting rings and they in turn formed resources, Yunnan University, Kunming 650091, constricting rings with three inflated-cells. Yunnan Province, PR China Key words: b-tubulin, evolution, fungi, phylogeny, Kevin D. Hyde predatory, systematics, rDNA Rajesh Jeewon Lei Cai INTRODUCTION Dhanasekaran Vijaykrishna Centre for Research in Fungal Diversity, Department of Nematode-trapping fungi can produce various trap- Ecology & Biodiversity, The University of Hong Kong, ping devices to capture nematodes and other Pokfulam Road, Hong Kong SAR, PR China microscopic animals (Duddington 1951a, b; Barron Keqin Zhang1 1977; Scholler et al 1999; Ahre´n et al 2004) and are Laboratory for Conservation and Utilization of Bio- important in biological control (Dong et al 2004). resources, Yunnan University, Kunming 650091, The three basic types of trapping devices are adhesive Yunnan Province, PR China knobs, constricting rings and adhesive networks and these can be subdivided further into seven types of trapping device (i.e., simple adhesive branches, Abstract: The systematic classification of nematode- unstalked adhesive knobs, stalked adhesive knobs, trapping fungi is redefined based on phylogenies nonconstricting rings, constricting rings, two-dimen- inferred from sequence analyses of 28S rDNA, 5.8S sional networks and three-dimensional networks rDNA and b-tubulin genes. Molecular data were (Rubner 1996)). The majority of nematode-trapping analyzed with maximum parsimony, maximum likeli- fungi are hyphomycetes, placed within the Orbiliales hood and Bayesian analysis. An emended generic (Orbiliomycetes) based on morphological and/or concept of nematode-trapping fungi is provided. molecular studies. Other examples include Nematoc- Arthrobotrys is characterized by adhesive networks, tonus concurrens Drechsler whose teleomorph be- Dactylellina by adhesive knobs, and Drechslerella by longs to the genus Hohenbuehelia (Basidiomycetes), constricting-rings. Phylogenetic placement of taxa which uses both adhesive traps and adhesive spores, characterized by stalked adhesive knobs and non- while Coprinus comatus (O.F. Mu¨ll) Gray and constricting rings also is confirmed in Dactylellina. Pleurotus ostreatus (Jacq.) Kumm. (Basidiomycetes) Species that produce unstalked adhesive knobs that produce toxins from specialized hyphal stalks to grow out to form loops are transferred from immobilize and digest the nematode (Barron and Gamsylella to Dactylellina, and those that produce unstalked adhesive knobs that grow out to form Thorn 1987, Dong et al 2004). networks are transferred from Gamsylella to Arthro- Since the pioneering work by Drechsler (1937), botrys. Gamsylella as currently circumscribed cannot nematode-trapping fungi have been classified in be treated as a valid genus. A hypothesis for the a number of genera based on morphology of conidia evolution of trapping-devices is presented based on (shape, septa and size) and conidiophores (branch- multiple gene data and morphological studies. ing, modifications of the apex). Traditional taxonom- Predatory and nonpredatory fungi appear to have ic concepts relied heavily on conidia and conidio- been derived from nonpredatory members of Orbilia. phore morphology without taking in account the The adhesive knob is considered to be the ancestral importance of trapping devices. This has led to type of trapping device from which constricting rings a situation where species with diverse types of and networks were derived via two pathways. In the trapping devices have been assigned to one genus, first pathway adhesive knobs retained their adhesive while others with similar trapping devices can be material forming simple two-dimension networks, found in different genera (Glockling and Dick 1994; eventually forming complex three-dimension net- Liu and Zhang 1994, 2003; Zhang et al 1996). works. In the second pathway adhesive knobs lost With molecular technology, traditional generic classification, generally based on the morphology of Accepted for publication 17 July 2005. conidial characters, was challenged. Rubner (1996) 1 Corresponding author. E-mail: [email protected] first used trapping structure to try to rationalize the 1034 LIETAL:NEMATODE-TRAPPING FUNGI 1035 classification of the nematode-trapping fungi, which The PCR reaction mixture consisted of 0.3 mL of 1.5 units was justified by the following molecular data. Phylog- of Taq DNA polymerase, 5 mLof103 buffer, 1.5 mLof enies based on rDNA sequences have indicated that 25 mm MgCl2, 4 mL of 2.5 mM dNTPs, 1.5 mLof10mm trapping devices are more informative than other primer, 3 mL of DNA template and made up to a final morphological characters in delimiting genera (Liou volume of 50 mL with double-distilled sterile water. PCR reaction were performed with these steps: 3 min at 95 C, 30 and Tzean 1997, Pfister 1997, Ahre´n et al 1998, cycles of 1 min at 94 C, 50 s at 52 C, 1 min at 72 C and Scholler et al 1999, Kano et al 2004). Ahre´n et al a final extension step of 10 min at 72 C. Amplified products (1998) found that nematode-tapping fungi clustered were electrophoresed on 1% agarose gels to check for size into three lineages: species with constricting rings, and purity. species with various adhesive structures (net, hyphae, Purified PCR products were sequenced directly on both knobs and nonconstricting rings) and species have no strands with the same primers that were used for amplifi- trapping devices. Based on results obtained from cation. Reactions were performed in an Applied Biosystem morphological and molecular characters, Hagedorn 3730 DNA Analyzer at the Genome Research Centre and Scholler (1999) and Scholler et al (1999) (University of Hong Kong). All the sequences have been classified nematode-trapping fungi into four genera: deposited in GenBank (TABLE I). Dactylellina characterized by stalked adhesive knobs Phylogenetic analysis.-DNA sequences were aligned with including species characterized by nonconstricting additional sequences obtained from GenBank (TABLE I) with BioEdit (Hall 1999) and Clustal X 1.83 (Thompson et rings and stalked adhesive knobs; Gamsylella charac- al 1997). Manual gap adjustments were made to improve terized by adhesive branches and unstalked knobs; the alignment. Phylogenetic analyses were conducted with Arthrobotrys characterized by adhesive networks; and PAUP* version 4.0b10 (Swofford 2002) and MrBayes 3.0b4 Drechslerella characterized by constricting rings. (Huelsenbeck and Ronquist 2001). Alignment gaps were In this study DNA sequences from 28S and 5.8S treated as missing data. The characters were weighted at rDNA and b-tubulin were analyzed to understand the different transition-transversion ratios (TTr) to determine evolution of trapping devices and further examine the most appropriate parameters giving the best trees. the relationships among nematode-trapping fungi. Maximum parsimony trees were found with 1000 heuristic Sequenced taxa were selected to provide evidence for: search and including parsimony-informative characters in (i) the evolution of trapping devices and (ii) the stepwise (random) addition and tree bisection and re- importance of adhesive branches, unstalked knobs, construction (TBR) as branch swapping algorithm. MAX- TREES were set to 5000, branches of zero length were stalked adhesive knobs and nonconstricting rings in collapsed and all most parsimonious trees were saved. the taxonomic placement of species. Branch support for all parsimony analyses was estimated by performing 1000 bootstrap replicates (Felsenstein 1985) MATERIALS AND METHODS with a heuristic search consisting of 10 random-addition replicates for each bootstrap replicate. Partition homoge- Morphological examination.—Isolates were cultured on neity test (Farris et al 1995, Huelsenbeck et al 1996), as cornmeal agar (CMA) at 25 C for 1 wk to check the implemented in PAUP, was performed to check whether characters of conidia and conidiophores. To verify the different genes could be combined. morphology of trapping devices cultures were cut into To select the best-fit model of evolution for the maximum small cubes and inoculated with the free-living nema- likelihood (ML) and Bayesian analyses, MrModeltest 2 tode, Paragrellus redivius (Linne) Goodey at 25 C for 3– (Posada and Crandall 1998, Nylander 2004) was used based 5 d (Duddington 1955, Wyborn et al 1969). All on a tree calculated under neighbor joining criterion under morphological characters were recorded and photo- the Jukes Cantor model (JC69) (Jukes and Cantor 1969). graphed. The mean measurement is based on 50 ML tree was built with a heuristic search, addition sequence counts. set to ‘‘as’’, with TBR branch swapping algorithm. Bayesian analyses were conducted with MrBayes 3.0b4. Markov chains DNA extraction.—Fungal cultures were grown 1 wk on were run for 1 000 000 generations and trees were sampled PDA at 25 C before DNA extraction. The mycelia were every 100th generation resulting in 10 000 trees. The burn- scraped from the surface of the agar and used as starting in number was determined by graphically visualizing the material. DNA was extracted with a modified CTAB likelihood scores. The first 1000 trees, which represented
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