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Evolution of Nematode-Trapping Cells of Predatory Fungi of the Orbiliaceae Based on Evidence from Rrna-Encoding DNA and Multiprotein Sequences

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Evolution of Nematode-Trapping Cells of Predatory Fungi of the Orbiliaceae Based on Evidence from Rrna-Encoding DNA and Multiprotein Sequences Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences Ying Yang†‡, Ence Yang†‡, Zhiqiang An§, and Xingzhong Liu†¶ †Key Laboratory of Systematic Mycology and Lichenology, Institute of Microbiology, Chinese Academy of Sciences 3A Datun Rd, Chaoyang District, Beijing 100101, China; ‡Graduate University of Chinese Academy of Sciences, Beijing 100049, China; and §Merck Research Laboratories, WP26A-4000, 770 Sumneytown Pike, West Point, PA 19486-0004 Communicated by Joan Wennstrom Bennett, Rutgers, The State University of New Jersey, New Brunswick, NJ, March 27, 2007 (received for review October 28, 2006) Among fungi, the basic life strategies are saprophytism, parasitism, These trapping devices all capture nematodes by means of an and predation. Fungi in Orbiliaceae (Ascomycota) prey on animals adhesive layer covering part or all of the device surfaces. The by means of specialized trapping structures. Five types of trapping constricting ring (CR), the fifth and most sophisticated trapping devices are recognized, but their evolutionary origins and diver- device (Fig. 1D) captures prey in a different way. When a gence are not well understood. Based on comprehensive phylo- nematode enters a CR, the three ring cells are triggered to swell genetic analysis of nucleotide sequences of three protein-coding rapidly inwards and firmly lasso the victim within 1–2 sec. genes (RNA polymerase II subunit gene, rpb2; elongation factor 1-␣ Phylogenetic analysis of ribosomal RNA gene sequences indi- ␣ gene, ef1- ; and ß tubulin gene, bt) and ribosomal DNA in the cates that fungi possessing the same trapping device are in the internal transcribed spacer region, we have demonstrated that the same clade (3, 8–11). Trapping devices are more informative initial trapping structure evolved along two lineages yielding two than asexual reproductive structures for grouping the nematode- distinct trapping mechanisms: one developed into constricting trapping fungi (4). Trapping devices remain inducible after many rings and the other developed into adhesive traps. Among adhe- years of culture on artificial media, suggesting that these highly sive trapping devices, the adhesive network separated from the differentiated structures are significant for the survival of these others early and evolved at a steady and gentle speed. The fungi. Various hypotheses on the evolution of trapping devices adhesive knob evolved through stalk elongation, with a final based on either morphological features or molecular characters development of nonconstricting rings. Our data suggest that the derived adhesive traps are at a highly differentiated stage. The have been proposed (2, 4, 9, 10), but conflicts exist between development of trapping devices is felicitous proof of adaptive molecular and phenotypic phylogenies. evolution. Although the generic classification of predatory fungi and their evolutionary lineage have been proposed based on phylo- Ascomycetes ͉ protein-coding genes ͉ molecular phylogeny ͉ fossil genetic analyses of rRNA-encoding DNA (rDNA) sequences, the relationship among fungi with adhesive trapping devices were not well resolved (3, 8–11). Because rDNA sequences redation plays a major role in energy and nutrient flow in the usually evolve slower than that of protein-coding genes (12), the Pbiological food chain. Carnivorism is best known from the animal kingdom, but the fungal kingdom has flesh eaters as well rDNA gene sequence was unable to answer all of the questions (1). Over 200 species of fungi (distributed in Zygomycota, on the relationships among this group of fungi (13–16). The Basidiomycota, and Ascomycota) use special structures to cap- protein-encoding genes such as RNA polymerase II subunit gene ␣ ␣ ture free-living nematodes in the soil (2). The most widespread (rpb2), elongation factor-1 gene (ef-1 ), and ß-tubulin gene (bt) predatory fungi are in the family of Orbiliaceae, Ascomycota (3, are involved in transcription, translation, and cytoskeleton, 4). Within a few hours of close contact with nematodes, the respectively (17, 18), and they have been widely used in phylo- sparse mycelia of these fungi will differentiate spontaneously genetic studies to resolve evolutionary questions that cannot be into functional structures (traps). The mycelial traps then adhere answered by rDNA genes. The combined use of internal tran- to, penetrate, kill, and digest the nematodes’ contents (5). To scribed spacer (ITS) rDNA and protein-coding genes allows understand the origin and evolution of these fascinating trapping improved understanding of the evolutionary events in different devices, it is essential to gain insights on how those novel devices life forms (19). The maximum likelihood (ML) method has been are differentiated, how nematode trapping fungi are related to successfully applied to reveal molecular evolution across diverse other organisms, and their reactions to the environments. taxa (20, 21). In this study, rDNA ITS region, protein-encoding Five kinds of trapping devices have been recognized and genes (rpb2, ef-1␣, and bt), and ML were used to trace the studied in predatory fungi of the orbiliaceous ascomycete family evolution of trapping devices in predatory fungi. (5–7). The adhesive network (AN), the most widely distributed trap, is formed by an erect lateral branch growing from a vegetative hypha, curving to fuse with the parent hypha and Author contributions: Y.Y. and E.Y. contributed equally to this work; Z.A. and X.L. designed developing more loops exterior to the original loop or on the research; Y.Y., E.Y., and X.L. performed research; Y.Y., E.Y., and X.L. contributed new EVOLUTION reagents/analytic tools; Y.Y., E.Y., Z.A., and X.L. analyzed data; and Y.Y., E.Y., Z.A., and X.L. parent hypha (Fig. 1A). The adhesive knob (AK) is a morpho- wrote the paper. logically distinct globose or subglobose cell that is either sessile The authors declare no conflict of interest. on the hypha or with an erect stalk. AK are normally closely Abbreviations: NCR, nonconstricting ring; CR, constricting ring; AC, adhesive column; AN, spaced along the hyphae (Fig. 1B). Nonconstricting rings (NCR) adhesive network; AK, adhesive knob; ML, maximum likelihood; ME, minimal evolution; always occur alongside AK, and are produced when erect lateral rDNA, rRNA-encoding DNA; BSV, bootstrap support value; ITS, internal transcribed spacer. branches from vegetative hypha thicken and curve to form a Data deposition: The sequences reported in this paper have been deposited in the GenBank generally three-celled ring that then fuses to the supporting stalk database (accession nos. are available in Table 1). (Fig. 1B). The adhesive column (AC) is a short erect branch ¶To whom correspondence should be addressed. E-mail: [email protected]. consisting of a few swollen cells produced on a hypha (Fig. 1C). © 2007 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0702770104 PNAS ͉ May 15, 2007 ͉ vol. 104 ͉ no. 20 ͉ 8379–8384 Fig. 1. Trapping devices of the Orbiliaceae. (A) AN. (B) AK with NCR. (C) AC. (D) CR. (Scale bar, 10 ␮m.) Results Phylogenetic Relationship of Trapping Devices. Cladograms based on parsimony analyses of nucleotide sequences of rDNA ITS regions (Fig. 2A) and the combined data set of four genes (ITS, bt, rpb, and ef1-␣) (Fig. 2B) revealed similar topological struc- tures [details of Fig. 2 can be obtained from TreeBASE (S1762)]. Fig. 2. Parsimony analyses of ITS regions (A) and combined data sets (B). The ML tree (Fig. 3) based on the combined data set of 2,706 Bootstrap values were obtained from 1,000 replications, and only Ͼ50% are bp provided more detailed information [high bootstrap values as shown. assessed by 1,000 minimal evolution (ME) bootstrap replica- tions] than the trees based on rDNA in the ITS region (Fig. 2A) were associated with NCR and are clustered into the other and revealed distinctive signatures that were diagnostic for subgroup with a 70% BSV (Fig. 3). different trapping devices. The data resulted in two main clades representing two different trapping mechanisms (adhesive and Ancestral State Reconstruction. Six characters (five trapping device nonadhesive). The nonadhesive clade [98% bootstrap support types and no traps), each with two states (present, absent), were value (BSV)] consists of species with CR and was paraphyleti- calculated by tracing all changes, and a tree with tree length of cally evolved with the adhesive clade, including trapping of knob, 8 was generated (Fig. 3). Evolution of the CR went through two stalked knob, hyphal column, NCR, and network. Evolution of stages. One was the formation of the stalks, and the other was the adhesive trapping structures with the same trapping mech- the formation of the rings. During evolution of the adhesive anism was resolved with the combined data-set tree. Two traps, each trap got one change from its ancestor. The primo- subclades corresponding to the AN (100% BSV) and other genitor of the trapping device first obtained adhesive strategy adhesive structures (63% BSV) were strongly supported. AC, and formed AN. Afterward, the evolution focused on covering AK, and AK associated with NCR grouped in the same subclade, one specialized cell (sessile knob or protuberance) with adhesive suggesting their close phylogenetic relationship (Fig. 3). materials. The protuberance proliferated to form the AC. The sessile knob developed an extended stalk to form stalked knob, Phylogenetic
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