Genome Studies on Nematophagous and Entomogenous Fungi in China
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Journal of Fungi Review Genome Studies on Nematophagous and Entomogenous Fungi in China Weiwei Zhang, Xiaoli Cheng, Xingzhong Liu and Meichun Xiang * State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, No. 3 Park 1, Beichen West Rd., Chaoyang District, Beijing 100101, China; [email protected] (W.Z.); [email protected] (X.C.); [email protected] (X.L.) * Correspondence: [email protected]; Tel.: +86-10-64807512; Fax: +86-10-64807505 Academic Editor: Luis V. Lopez-Llorca Received: 9 December 2015; Accepted: 29 January 2016; Published: 5 February 2016 Abstract: The nematophagous and entomogenous fungi are natural enemies of nematodes and insects and have been utilized by humans to control agricultural and forestry pests. Some of these fungi have been or are being developed as biological control agents in China and worldwide. Several important nematophagous and entomogenous fungi, including nematode-trapping fungi (Arthrobotrys oligospora and Drechslerella stenobrocha), nematode endoparasite (Hirsutella minnesotensis), insect pathogens (Beauveria bassiana and Metarhizium spp.) and Chinese medicinal fungi (Ophiocordyceps sinensis and Cordyceps militaris), have been genome sequenced and extensively analyzed in China. The biology, evolution, and pharmaceutical application of these fungi and their interacting with host nematodes and insects revealed by genomes, comparing genomes coupled with transcriptomes are summarized and reviewed in this paper. Keywords: fungal genome; biological control; nematophagous; entomogenous 1. Introduction Nematophagous fungi infect their hosts using traps and other devices such as adhesive conidia and parasitic hyphae tips [1,2]. Entomogenous fungi are associated with insects, mainly as pathogens or parasites [3]. Both nematophagous and entomogenous fungi are important biocontrol resources [1,3]. Cordyceps spp. are ancient resources in Chinese medicine [4]. Biological control is an economically and ecologically friendly approach for controlling nematode and insect pests that have a negative economic impact in agriculture [5]. Nematophagous and entomopathogenic fungi have been used with various strategies for almost a century and, for instance, mass production of entomopathogenic fungi were utilized for insect-pest control in the field while nematophagous fungi were released to the soil for nematode control [6,7]. There is also a long history of utilizing these fungi for the control of agricultural and forestry pests in China [8]. Among these fungi, Arthrobotrys oligospora (adhesive network traps) and Drechslerella stenobrocha (constricting ring trap) are well-known nematode trapping fungi in the Orbiliales (Orbiliomycetes and Ascomycota) [9–11]; Hirsutella minnesotensis, as a nematode endoparasite, responds to the natural suppressiveness of soybean cyst nematode [12–14]; Ophiocordyceps sinensis, a famous fungus used as a traditional Chinese medicine, belongs to Ophiocordycipitaceae, Hypocreales (Sordariomycetes, Ascomycota) [15]; Cordyceps militaris as medicinal fungus and Beauveria bassiana as biocontrol agent of insect are representatives of Cordycipitaceae, Hypocreales (Sordariomycetes, Ascomycota) [16,17]; and Metarhizium spp. in Clavicipitaceae, Hypocreales (Sordariomycetes, Ascomycota) are important entomopathogens [18]. The biology, evolution, interaction with hosts, biocontrol application for pests, and medicinal use of these fungi have been extensively studied by Chinese mycologists [19,20]. J. 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A numberbiological of nematophagous issues of those andfungi entomogenous and their sophisticated fungi extensively mechanisms studied for in interacting China have with been their genome sequencedinvertebrate by Chinese hosts. mycologistsA number of [ 9nematophagous,10,13,15–18]. The and approaches entomogenous obtained fungi fromextensively analysis studied of genomes, in andChina comparing have genomesbeen genome and transcriptomes sequenced by ofChinese these fungi,mycologists provide [9,10,13,15 comprehensive–18]. The understanding approaches of theirobtained biology from and interactionanalysis of withgenomes, invertebrate and comparing hosts, andgenomes furthermore, and transcriptomes enhance their of these application fungi, in pestprovide control comprehensive and medicine utilization.understanding of their biology and interaction with invertebrate hosts, and furthermore, enhance their application in pest control and medicine utilization. 2. Nematophagous Fungi 2. Nematophagous Fungi Nematophagous fungi can use specialized traps to capture nematodes, conidia to adhere to nematodes,Nematophagous hyphae tips fungi to parasitize can use specialized nematode traps females to capture and eggs,nematodes, or produce conidia toxinsto adhere to attackto nematodes, hyphae tips to parasitize nematode females and eggs, or produce toxins to attack nematodes [2]. Nematode-trapping fungi and nematode endoparasitic fungi are two important groups nematodes [2]. Nematode‐trapping fungi and nematode endoparasitic fungi are two important of nematophagous fungi. Predation is one of the fungal life-strategies to destroy nematodes [1,23] groups of nematophagous fungi. Predation is one of the fungal life‐strategies to destroy nematodes by capturing nematodes with sophisticated trapping structures, including constricting rings and [1,23] by capturing nematodes with sophisticated trapping structures, including constricting rings severaland other several types other of types adhesive of adhesive traps (sessiletraps (sessile adhesive adhesive knobs, knobs, stalked stalked adhesive adhesive knobs, knobs, adhesive adhesive nets, adhesivenets, adhesive columns, columns, and non-constricting and non‐constricting rings) (Figure rings) 1(FigureA–D) [ 1A–D)24,25]. [24,25]. The traps The are traps usually are usually produced fromproduced hyphae from and hyphae induced and by induced nematodes, by nematodes, peptides, peptides, and nematode and nematode extracts extracts [26 ,[26,27].27]. Most Most ofof the nematode-trappingthe nematode‐trapping fungi belong fungi tobelong Orbiliales to Orbiliales (Ascomycota). (Ascomycota). Among Among these fungi, these Arthrobotrysfungi, Arthrobotrys oligospora formingoligospora adhesive forming nets adhesive was firstnets was genome first genome sequenced sequenced to understand to understand the the molecular molecular basis basis ofof the mechanismsthe mechanisms for capturing for capturing nematodes nematodes (Table (Table1)[ 28 ,1)29 [28,29].]. A proposed A proposed model model containing containing multiple multiple fungal signalfungal transduction signal transduction pathways associatedpathways associated with diverse with cellular diverse processes cellular processes such as energy such as metabolism, energy biosynthesismetabolism, of the biosynthesis cell wall and of the adhesive cell wall proteins, and adhesive cell division, proteins, glycerol cell division, accumulation, glycerol accumulation, and peroxisome biogenesisand peroxisome [29]. The followingbiogenesis sequenced[29]. The following genome bysequenced Chinese mycologistsgenome by Chinese was Drechslerella mycologists stenobrocha was , Drechslerella stenobrocha, which forms constricting rings to actively capture nematodes. Comparative which forms constricting rings to actively capture nematodes. Comparative genomic analysis provided genomic analysis provided support for the hypothesis that nematode trapping fungi evolved from support for the hypothesis that nematode trapping fungi evolved from saprophytic fungi in a high saprophytic fungi in a high carbon and low nitrogen environment and revealed the transition carbonbetween and low saprophagy nitrogen environmentand predation and for revealed further the understanding transition between of the saprophagy interaction and between predation for furthernematode understanding‐trapping fungi of and the nematodes interaction [30]. between nematode-trapping fungi and nematodes [30]. Figure 1. Morphology of traps and adhesive conidia produced by nematophagous fungi: (A) Figure 1. Morphology of traps and adhesive conidia produced by nematophagous fungi: (A) Adhesive Adhesive nets (Arthrobotrys oligospora); (B) Constricting rings (Drechslerella stenobrocha); (C) nets (Arthrobotrys oligospora); (B) Constricting rings (Drechslerella stenobrocha); (C) Adhesive columns Adhesive columns (Gamsylella cionopaga); (D) Adhesive knobs (Gamsylella robusta); and (E, F) (Gamsylella cionopaga); (D) Adhesive knobs (Gamsylella robusta); and (E, F) Adhesive conidia Adhesive conidia (Hirsutella minnesotensis). Bars = 10 μm. (Hirsutella minnesotensis). Bars = 10 µm. J. Fungi 2016, 2, 9 3 of 14 Table 1. Available genomic sequences nematophagous fungi in China. Nematode Nematode-Trapping Fungi Entomogenous