Abstract
Nematode-trapping fungi develop complex trapping devices to capture and consume nematodes. The dynamics of these organisms is especially important given the pathogenicity of nematodes and, consequently, the potential application of nematode-trapping fungi as biocontrol agents. Furthermore, both the nematodes and nematode-trapping fungi can be easily grown in laboratories, making them a unique manipulatable predator-prey system to study their coevolution. Several different aspects of these fungi have been studied, such as their genetics and the different factors triggering trap formation. In this review, we use the nematode-trapping fungus Arthrobotrys oligospora (which forms adhesive nets) as a model to describe the trapping process. We divide this process into several stages; namely attraction, recognition, trap formation, adhesion, penetration, and digestion. We summarize the latest findings in the field and current knowledge on the interactions between nematodes and nematode-trapping fungi, representing both sides of the predator-prey interaction.
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References
Åhman J, Johansson T, Olsson M, Punt PJ, Van den Hondel CAMJJ, Tunlid A (2002) Improving the pathogenicity of a nematode-trapping fungus by genetic engineering of a subtilisin with nematotoxic activity. Appl Environ Microbiol 68(7):3408–3415. https://doi.org/10.1128/AEM.68.7.3408-3415.2002
Ahrén D, Tholander M, Fekete C, Rajashekar B, Friman E, Johansson T, Tunlid A (2005) Comparison of gene expression in trap cells and vegetative hyphae of the nematophagous fungus Monacrosporium haptotylum. Microbiol-Uk 151(3):789–803. https://doi.org/10.1099/mic.0.27485-0
Ahrén D, Tunlid A (2003) Evolution of parasitism in nematode-trapping fungi. J Nematol 35(2):194–197
Ahrén D, Ursing BM, Tunlid A (1998) Phylogeny of nematode-trapping fungi based on 18S rDNA sequences. FEMS Microbiol Lett 158(2):179–184. https://doi.org/10.1016/S0378-1097(97)00519-3
Andersson K-M, Kumar D, Bentzer J, Friman E, Ahrén D, Tunlid A (2014) Interspecific and host-related gene expression patterns in nematode-trapping fungi. BMC Genomics 15:968. https://doi.org/10.1186/1471-2164-15-968
Back MA, Haydock PPJ, Jenkinson P (2002) Disease complexes involving plant parasitic nematodes and soilborne pathogens. Plant Pathol 51:683–697. https://doi.org/10.1046/j.1365-3059.2002.00785.x
Balan J, Križková L, Nemec P, Vollek V (1974) Production of nematode-attracting and nematicidal substances by predacious fungi. Folia Microbiol 19(6):512–519. https://doi.org/10.1007/BF02872918
Balogh J, Tunlid A, Rosén S (2003) Deletion of a lectin gene does not affect the phenotype of the nematode-trapping fungus Arthrobotrys oligospora. Fungal Genet Biol 39(2):128–135. https://doi.org/10.1016/s1087-1845(03)00023-9
Barron GL (2003) Predatory fungi, wood decay, and the carbon cycle. Biodiversity 4(1):3–9. https://doi.org/10.1080/14888386.2003.9712621
Bartnicki-Garcia S, Eren J, Pramer D (1964) Carbon dioxide-dependent morphogenesis in Arthrobotrys conoides. Nature 204(4960):804–804. https://doi.org/10.1038/204804a0
Baynes MA, Russell DM, Newcombe G, Carta LK, Rossman AY, Ismaiel A (2012) A mutualistic interaction between a fungivorous nematode and a fungus within the endophytic community of Bromus tectorum. Fungal Ecol 5(5):610–623. https://doi.org/10.1016/j.funeco.2012.03.004
Berg M, Stenuit B, Ho J, Wang A, Parke C, Knight M, Alvarez-Cohen L, Shapira M (2016) Assembly of the Caenorhabditis elegans gut microbiota from diverse soil microbial environments. Isme J 10(8):1998–2009. https://doi.org/10.1038/ismej.2015.253
Blaxter ML, Page AP, Rudin W, Maizels RM (1992) Nematode surface coats: actively evading immunity. Parasitol Today 8(7):243–247. https://doi.org/10.1016/0169-4758(92)90126-M
Boddy L (1999) Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91(1):13–32. https://doi.org/10.2307/3761190
Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14(6):224–228. https://doi.org/10.1016/s0169-5347(98)01583-3
Butcher RA, Fujita M, Schroeder FC, Clardy J (2007) Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat Chem Biol 3(7):420–422. https://doi.org/10.1038/nchembio.2007.3
Choe A, von Reuss SH, Kogan D, Gasser RB, Platzer EG, Schroeder FC, Sternberg PW (2012) Ascaroside signaling is widely conserved among nematodes. Curr Biol 22(9):772–780. https://doi.org/10.1016/j.cub.2012.03.024
Cox GN, Kusch M, Edgar RS (1981) Cuticle of Caenorhabditis elegans: its isolation and partial characterization. J Cell Biol 90(1):7–17. https://doi.org/10.1083/jcb.90.1.7
Dirksen P, Marsh SA, Braker I, Heitland N, Wagner S, Nakad R, Mader S, Petersen C, Kowallik V, Rosenstiel P, Felix MA, Schulenburg H (2016) The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model. BMC Biol 14:38. https://doi.org/10.1186/s12915-016-0258-1
Ewbank JJ, Pujol N (2016) Local and long-range activation of innate immunity by infection and damage in C. elegans. Curr Opin Immunol 38:1–7. https://doi.org/10.1016/j.coi.2015.09.005
Field JI, Webster J (1977) Traps of predacious fungi attract nematodes. T Brit Mycol Soc 68(Jun):467–469
Friman E, Olsson S, Nordbring-Hertz B (1985) Heavy trap formation by Arthrobotrys oligospora in liquid culture. FEMS Microbiol Ecol 31(1):17–21. https://doi.org/10.1016/0378-1097(85)90042-4
Giannakis N, Sanders FE (1990) Interactions between mycophagous nematodes, mycorrhizal and other soil fungi. Agric Ecosyst Environ 29:163–167. https://doi.org/10.1016/0167-8809(90)90270-N
Gray NF (1983) Ecology of nematophagous fungi: distribution and habitat. Ann Appl Biol 102(3):501–509. https://doi.org/10.1111/j.1744-7348.1983.tb02721.x
Grønvold J, Wolstrup J, Nansen P, Henriksen SA, Larsen M, Bresciani J (1993) Biological control of nematode parasites in cattle with nematode-trapping fungi: a survey of Danish studies. Vet Parasitol 48:311–325. https://doi.org/10.1016/0304-4017(93)90165-J
Hasna MK, Insunza V, Lagerlöf J, Rämert B (2007) Food attraction and population growth of fungivorous nematodes with different fungi. Ann Appl Biol 151(2):175–182. https://doi.org/10.1111/j.1744-7348.2007.00163.x
Herrera-Estrella A, Casas-Flores S, Kubicek CP (2016) Nematophagous fungi. In: Kubicek C, Druzhinina I (eds) Environmental and microbial relationships the Mycota, vol 4. Springer, Berlin, Heidelberg, pp 247–267
Hsueh YP, Gronquist MR, Schwarz EM, Nath RD, Lee CH, Gharib S, Schroeder FC, Sternberg PW (2017) Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and food to lure its nematode prey. elife 6. https://doi.org/10.7554/eLife.20023
Hsueh YP, Mahanti P, Schroeder FC, Sternberg PW (2013) Nematode-trapping fungi eavesdrop on nematode pheromones. Curr Biol 23(1):83–86. https://doi.org/10.1016/j.cub.2012.11.035
Idnurm A, Bailey AM, Cairns TC, Elliott CE, Foster GD, Ianiri G, Jeon J (2017) A silver bullet in a golden age of functional genomics: the impact of agrobacterium-mediated transformation of fungi. Fungal Biol Biotechnol 4:6. https://doi.org/10.1186/s40694-017-0035-0
Jaffee BA (2003) Correlations between most probable number and activity of nematode-trapping fungi. Phytopathology 93(12):1599–1605
Jansson HB (1982) Predacity by nematophagous fungi and its relation to the attraction of nematodes. Microb Ecol 8(3):233–240. https://doi.org/10.1007/BF02011427
Jiang D, Zhou J, Bai G, Xing X, Tang L, Yang X, Li J, Zhang KQ, Yang J (2017a) Random mutagenesis analysis and identification of a novel C2H2-type transcription factor from the nematode-trapping fungus Arthrobotrys oligospora. Sci Rep 7(1):5640. https://doi.org/10.1038/s41598-017-06075-5
Jiang X, Xiang M, Liu X (2017b) Nematode-trapping fungi. Microbiol Spectr 5(1):1–12. https://doi.org/10.1128/microbiolspec.FUNK-0022-2016
Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG, Kikuchi T, Manzanilla-Lopez R, Palomares-Rius JE, Wesemael WM, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14(9):946–961. https://doi.org/10.1111/mpp.12057
Kim DH, Ewbank JJ (2015) Signaling in the innate immune response. WormBook:1–51 doi:https://doi.org/10.1895/wormbook.1.83.2
Kim DH, Feinbaum R, Alloing G, Emerson FE, Garsin DA, Inoue H, Tanaka-Hino M, Hisamoto N, Matsumoto K, Tan MW, Ausubel FM (2002) A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297(5581):623–626. https://doi.org/10.1126/science.1073759
Lawton (nee Ress) J.R. JR (1957) The formation of constricting rings in nematode-catching hyphomycetes grown in pure culture. J Exp Bot 8(1):50–54. https://doi.org/10.1093/jxb/8.1.50
Li L, Ma M, Liu Y, Zhou J, Qu Q, Lu K, Fu D, Zhang K (2011) Induction of trap formation in nematode-trapping fungi by a bacterium. FEMS Microbiol Lett 322(2):157–165. https://doi.org/10.1111/j.1574-6968.2011.02351.x
Li L, Yang M, Luo J, Qu Q, Chen Y, Liang L, Zhang K (2016) Nematode-trapping fungi and fungus-associated bacteria interactions: the role of bacterial diketopiperazines and biofilms on Arthrobotrys oligospora surface in hyphal morphogenesis. Environ Microbiol 18(11):3827–3839. https://doi.org/10.1111/1462-2920.13340
Li Y, Hyde KD, Jeewon R, Cai L, Vijaykrishna D, Zhang K (2005) Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes. Mycologia 97(5):1034–1046. https://doi.org/10.3852/mycologia.97.5.1034
Liang L, Shen R, Mo Y, Yang J, Ji X, Zhang KQ (2015) A proposed adhesin AoMad1 helps nematode-trapping fungus Arthrobotrys oligospora recognizing host signals for life-style switching. Fungal Genet Biol 81:172–81. https://doi.org/10.1016/j.fgb.2015.02.012
Liu K, Tian J, Xiang M, Liu X (2012) How carnivorous fungi use three-celled constricting rings to trap nematodes. Protein Cell 3(5):325–328. https://doi.org/10.1007/s13238-012-2031-8
Liu K, Zhang W, Lai Y, Xiang M, Wang X, Zhang X, Liu X (2014) Drechslerella stenobrocha genome illustrates the mechanism of constricting rings and the origin of nematode predation in fungi. BMC Genomics 15:114. https://doi.org/10.1186/1471-2164-15-114
Liu X, Xiang M, Che Y (2009) The living strategy of nematophagous fungi. Mycoscience 50(1):20–25. https://doi.org/10.1007/s10267-008-0451-3
Lopez-Llorca LV, Maciá-Vicente JG, Jansson HB (2007) Mode of action and interactions of Nematophagous fungi. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Integrated Management of Plant Pests and Diseases, vol 2. Springer Netherlands, Dordrecht, The Netherlands, pp 51–76
Magan N (2007) Fungi in Extreme Environments. In: Kubicek C, Druzhinina I (eds) Environmental and microbial relationships the Mycota, vol 4. Springer, Berlin, Heidelberg
Martin MJ, Riedel RM, Rowe RC (1982) Verticillium dahliae and Pratylenchus penetrans - interactions in early dying complex of potato in Ohio. Phytopathology 72(6):640–644. https://doi.org/10.1094/Phyto-77-640
McSorley R (2003) Adaptations of nematodes to environmental extremes. Fla Entomol 86(2):138–142. https://doi.org/10.1653/0015-4040(2003)086[0138:aontee]2.0.co;2
Meerupati T, Andersson KM, Friman E, Kumar D, Tunlid A, Ahrén D (2013) Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLoS Genet 9(11):e1003909. https://doi.org/10.1371/journal.pgen.1003909
Nicholas HR, Hodgkin J (2004) The ERK MAP kinase cascade mediates tail swelling and a to rectal infection protective response in C. elegans. Curr Biol 14(14):1256–1261. https://doi.org/10.1016/j.cub.2004.07.022
Niu X-M, Zhang K-Q (2011) Arthrobotrys oligospora: a model organism for understanding the interaction between fungi and nematodes. Mycology 2(2):59–78. https://doi.org/10.1080/21501203.2011.562559
Nordbring-Hertz B (1973) Peptide-induced morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora. Physiol Plant 29(2):223–233. https://doi.org/10.1111/j.1399-3054.1973.tb03097.x
Nordbring-Hertz B (2004) Morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora—an extensive plasticity of infection structures. Mycologist 18(3):125–133. https://doi.org/10.1017/S0269915X04003052
Nordbring-Hertz B, Friman E, Veenhuis M (1989) Hyphal fusion during initial stages of trap formation in Arthrobotrys oligospora. A Van Leeuw J Microb 55(3):237–244
Nordbring-Hertz B, Jansson H-B, Tunlid A (2011) Nematophagous fungi eLS. John Wiley & Sons, Ltd, Chichester, pp 1–13
Nordbring-Hertz B, Mattiasson B (1979) Action of a nematode-trapping fungus shows lectin-mediated host–microorganism interaction. Nature 281(5731):477–479. https://doi.org/10.1038/281477a0
Nordbring-Hertz B, Veenhuis M, Harder W (1984) Dialysis membrane technique for ultrastructural studies of microbial interactions. Appl Environ Microbiol 47(1):195–197
Page AP, Johnstone IL (2007) The cuticle. WormBook:1–15 doi:https://doi.org/10.1895/wormbook.1.138.1
Perry RN, Moens M (2011) Survival of parasitic nematodes outside the host. In: Perry RN, Wharton DA (eds) Molecular and physiological basis of nematode survival. CABI, Wallingford, pp 1–27
Persmark L, Nordbring-Hertz B (2006) Conidial trap formation of nematode-trapping fungi in soil and soil extracts. FEMS Microbiol Ecol 22(4):313–323. https://doi.org/10.1111/j.1574-6941.1997.tb00383.x
Platt HM, Shaw KM, Lambshead PJD (1984) Nematode species abundance patterns and their use in the detection of environmental perturbations. Hydrobiologia 118:59–66. https://doi.org/10.1007/BF00031788
Pramer D, Stoll NR (1959) Nemin: a morphogenic substance causing trap formation by predaceous fungi. Science 129(3354):966–967
Pujol N, Zugasti O, Wong D, Couillault C, Kurz CL, Schulenburg H, Ewbank JJ (2008) Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog 4(7):e1000105. https://doi.org/10.1371/journal.ppat.1000105
Rosen S, Sjollema K, Veenhuis M, Tunlid A (1997) A cytoplasmic lectin produced by the fungus Arthrobotrys oligospora functions as a storage protein during saprophytic and parasitic growth. Microbiol-Uk 143:2593–2604. https://doi.org/10.1099/00221287-143-8-2593
Saxena G, Dayal R, Mukerji KG (1987) Interaction of nematodes with nematophagus fungi: induction of trap formation, attraction and detection of attractants. FEMS Microbiol Lett 45(6):319–327. https://doi.org/10.1016/0378-1097(87)90018-8
Schenck NC, Graham SO, Green NE (1975) Temperature and light effect on contamination and spore germination of vesicular-arbuscular mycorrhizal fungi. Mycologia 67(6):1189–1192
Scholler M, Rubner A (1994) Predacious activity of the nematode-destroying fungus Arthrobotrys oligospora in dependence of the medium composition. Microbiol Res 149(2):145–149. https://doi.org/10.1016/S0944-5013(11)80110-2
Shi TQ, Liu GN, Ji RY, Shi K, Song P, Ren LJ, Huang H, Ji XJ (2017) CRISPR/Cas9-based genome editing of the filamentous fungi: the state of the art. Appl Microbiol Biotechnol 101(20):7435–7443. https://doi.org/10.1007/s00253-017-8497-9
Smith ML, Bruhn JN, Anderson JB (1992) The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356:428–431. https://doi.org/10.1038/356428a0
Song TY, Xu ZF, Chen YH, Ding QY, Sun YR, Miao Y, Zhang KQ, Niu XM (2017) Potent nematicidal activity and new hybrid metabolite production by disruption of a cytochrome P450 gene involved in the biosynthesis of morphological regulatory Arthrosporols in nematode-trapping fungus Arthrobotrys oligospora. J Agric Food Chem 65(20):4111–4120. https://doi.org/10.1021/acs.jafc.7b01290
Srinivasan J, Kaplan F, Ajredini R, Zachariah C, Alborn HT, Teal PEA, Malik RU, Edison AS, Sternberg PW, Schroeder FC (2008) A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 454(7208):1115–1U46
Sternberg PW (2017) In retrospect: forty years of cellular clues from worms. Nature 543(7647):628–630. https://doi.org/10.1038/543628a
Su H, Zhao Y, Zhou J, Feng H, Jiang D, Zhang KQ, Yang J (2017) Trapping devices of nematode-trapping fungi: formation, evolution, and genomic perspectives. Biol Rev Camb Philos Soc 92(1):357–368. https://doi.org/10.1111/brv.12233
Tan MW, Ausubel FM (2000) Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. Curr Opin Microbiol 3(1):29–34. https://doi.org/10.1016/S1369-5274(99)00047-8
Tan MW, Rahme LG, Sternberg JA, Tompkins RG, Ausubel FM (1999) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. P Natl Acad Sci USA 96(5):2408–2413. https://doi.org/10.1073/pnas.96.5.2408
Tosi S, Annovazzi L, Tosi I, Iadarola P, Caretta G (2002) Collagenase production in an antarctic strain of Arthrobotrys tortor Jarowaja. Mycopathologia 153(3):157–162. https://doi.org/10.1023/A:1014511105803
Tunlid A, Jansson HB, Nordbring-Hertz B (1992) Fungal attachment to nematodes. Mycol Res 96(6):401–412. https://doi.org/10.1016/S0953-7562(09)81082-4
Tunlid A, Johansson T, Nordbring-Hertz B (1991) Surface polymers of the nematode-trapping fungus Arthrobotrys oligospora. J Gen Microbiol 137(6):1231–1240. https://doi.org/10.1099/00221287-137-6-1231
Tunlid A, Rosén S, Ek B, Rask L (1994) Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Arhtrobotrys oligospora. Microbiol-Uk 140:1687–1695. https://doi.org/10.1099/13500872-140-7-1687
van der Putten WH, Cook R, Costa S, Davies KG, Fargette M, Freitas H, Hol WHG, Kerry BR, Maher N, Mateille T, Moens M, de la Peña E, Piśkiewicz AM, Raeymaekers ADW, Rodríguez-Echeverría S, van der Wurff AWG (2006) Nematode interactions in nature: models for sustainable control of nematode pests of crop plants? Adv Agron 89:227–260. https://doi.org/10.1016/S0065-2113(05)89005-4
Van Gundy SD, Kirkpatrick JD, Golden J (1977) The nature and role of metabolic leakage from root-knot nematode galls and infection by Rhizoctonia solani. J Nematol 9(2):113–121
Veenhuis M, Nordbring-Hertz B, Harder W (1985a) Development and fate of electron-dense microbodies in trap cells of the nematophagous fungus Arthrobotrys oligospora. A Van Leeuw J Microb 51(4):399–407. https://doi.org/10.1007/BF02275044
Veenhuis M, Nordbring-Hertz B, Harder W (1985b) An electron-microscopical analysis of capture and initial stages of penetration of nematodes by Arthrobotrys oligospora. A Van Leeuw J Microb 51(4):385–398
Veenhuis M, Van Wijk C, Wyss U, Nordbring-Hertz B, Harder W (1989) Significance of electron dense microbodies in trap cells of the nematophagous fungus Arthrobotrys oligospora. A Van Leeuw J Microb 56(3):251–261
Vidal-Diez de Ulzurrun G, Baetens JM, Van den Bulcke J, Lopez-Molina C, De Windt I, De Baets B (2015) Automated image-based analysis of spatio-temporal fungal dynamics. Fungal Genet Biol 84:12–25. https://doi.org/10.1016/j.fgb.2015.09.004
Walker NR, Kirkpatrick TL, Rothrock CS (1998) Interaction between Meloidogyne incognita and Thielaviopsis basicola on cotton (Gossypium hirsutum). J Nematol 30(4):415–422
Waller PJ, Larsen M (1993) The role of nematophagous fungi in the biological control of nematode parasites of livestock. Int J Parasitol 23(4):539–546. https://doi.org/10.1016/0020-7519(93)90044-Y
Wang R, Wang J, Yang X (2015) The extracellular bioactive substances of Arthrobotrys oligospora during the nematode-trapping process. Biol Control 86:60–65. https://doi.org/10.1016/j.biocontrol.2015.04.003
Wang RB, Yang JK, Lin C, Zhang Y, Zhang KQ (2006) Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Dactylella shizishanna. Lett Appl Microbiol 42(6):589–594. https://doi.org/10.1111/j.1472-765X.2006.01908.x
Wang X, Li G-H, Zou C-G, Ji X-L, Liu T, Zhao P-J, Liang L-M, Xu J-P, An Z-Q, Zheng X, Qin Y-K, Tian M-Q, Xu Y-Y, Ma Y-C, Yu Z-F, Huang X-W, Liu S-Q, Niu X-M, Yang J-K, Huang Y, Zhang K-Q (2014) Bacteria can mobilize nematode-trapping fungi to kill nematodes. Nat Commun 5:5776. https://doi.org/10.1038/ncomms6776
Warcup JH (1957) Studies on the occurrence and activity of fungi in a wheat-field soil. T Brit Mycol Soc 40(2):237–259. https://doi.org/10.1016/S0007-1536(57)80010-2
Xie H, Aminuzzaman FM, Xu L, Lai Y, Li F, Liu X (2010) Trap induction and trapping in eight nematode-trapping fungi (Orbiliaceae) as affected by juvenile stage of Caenorhabditis elegans. Mycopathologia 169(6):467–473. https://doi.org/10.1007/s11046-010-9279-4
Xu LL, Lai YL, Wang L, Liu XZ (2011) Effects of abscisic acid and nitric oxide on trap formation and trapping of nematodes by the fungus Drechslerella stenobrocha AS6.1. Fungal Biol 115(2):97–101. https://doi.org/10.1016/j.funbio.2010.10.006
Xu ZF, Wang BL, Sun HK, Yan N, Zeng ZJ, Zhang KQ, Niu XM (2015) High trap formation and low metabolite production by disruption of the polyketide synthase gene involved in the biosynthesis of Arthrosporols from nematode-trapping fungus Arthrobotrys oligospora. J Agric Food Chem 63(41):9076–82. https://doi.org/10.1021/acs.jafc.5b04244
Yang E, Xu L, Yang Y, Zhang X, Xiang M, Wang C, An Z, Liu X (2012) Origin and evolution of carnivorism in the Ascomycota (fungi). P Natl Acad Sci USA 109(27):10960–10965. https://doi.org/10.1073/pnas.1120915109
Yang J, Tian B, Liang L, Zhang KQ (2007a) Extracellular enzymes and the pathogenesis of nematophagous fungi. Appl Microbiol Biotechnol 75(1):21–31. https://doi.org/10.1007/s00253-007-0881-4
Yang J, Wang L, Ji X, Feng Y, Li X, Zou C, Xu J, Ren Y, Mi Q, Wu J, Liu S, Liu Y, Huang X, Wang H, Niu X, Li J, Liang L, Luo Y, Ji K, Zhou W, Yu Z, Li G, Liu Y, Li L, Qiao M, Feng L, Zhang KQ (2011) Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathog 7(9):1–12. https://doi.org/10.1371/journal.ppat.1002179
Yang Y, Yang E, An Z, Liu X (2007b) Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. P Natl Acad Sci USA 104(20):8379–8384. https://doi.org/10.1073/pnas.0702770104
Zhao X, Wang Y, Zhao Y, Huang Y, Zhang KQ, Yang J (2014) Malate synthase gene AoMls in the nematode-trapping fungus Arthrobotrys oligospora contributes to conidiation, trap formation, and pathogenicity. App Microbiol Biotechnol 98(6):2555–2563
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We thank Tsong-Yu Huang for his original drawing in the figure and John Wang and Ting-Fan Wang for giving comments on the manuscript.
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This research was funded by the Ministry of Science and Technology of Taiwan (grant number 106-2311-B-001-039-MY3).
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Vidal-Diez de Ulzurrun, G., Hsueh, YP. Predator-prey interactions of nematode-trapping fungi and nematodes: both sides of the coin. Appl Microbiol Biotechnol 102, 3939–3949 (2018). https://doi.org/10.1007/s00253-018-8897-5
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DOI: https://doi.org/10.1007/s00253-018-8897-5