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RNA-Seq reveals the molecular mechanism of trapping and killing of root-knot nematodes by nematode-trapping fungi

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Abstract

Nematode-trapping fungi are well known for their inherent potential to trap and kill nematodes using specialized trapping devices. However, the molecular mechanisms underlying the trapping and subsequent processes are still unclear. Therefore, in this study, we examined differential genes expression in two nematode-trapping fungi after baiting with nematode extracts. In Arthrobotrys conoides, 809 transcripts associated with diverse functions such as signal transduction, morphogenesis, stress response and peroxisomal proteins, proteases, chitinases and genes involved in the host-pathogen interaction showed differential expression with fold change (>±1.5 fold) in the presence of nematode extract with FDR (p-value < 0.001). G-proteins and mitogen activated protein kinases are considered crucial for signal transduction mechanism. Results of qRT-PCR of 20 genes further validated the sequencing data. Further, variations in gene expression among Duddingtonia flagrans and A. conoides showed septicity of nematode-trapping fungi for its host. The findings illustrate the molecular mechanism of fungal parasitism in A. conoides which may be helpful in developing a potential biocontrol agent against parasitic nematodes.

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References

  • Ahren D, Tunlid A (2003) Evolution of parasitism in nematode-trapping fungi. J Nematol 35(2):194–197

    CAS  Google Scholar 

  • Ahren 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. Microbiology 151(3):789–803. doi:10.1099/mic.0.27485-0

    Article  Google Scholar 

  • Al-Hazmi AS, Schmitt DP, Sasser JN (1982) The effect of Arthrobotrys conoides on Meloidogyne incognita population densities in corn as influenced by temperature, fungus inoculum density, and time of fungus introduction in the soil. J Nematol 14(2):168–173

    CAS  Google Scholar 

  • Alvarez-Tabares I, Perez-Martin J (2010) Septins from the phytopathogenic fungus Ustilago maydis are required for proper morphogenesis but dispensable for virulence. PloS ONE 5(9):e12933. doi:10.1371/journal.pone.0012933

    Article  Google Scholar 

  • Andersson KM, Meerupati T, Levander F, Friman E, Ahren D, Tunlid A (2013) Proteome of the nematode-trapping cells of the fungus Monacrosporium haptotylum. Appl Environ Microbiol 79(16):4993–5004. doi:10.1128/AEM.01390-13

    Article  CAS  Google Scholar 

  • Andersson KM, Kumar D, Bentzer J, Friman E, Ahren D, Tunlid A (2014) Interspecific and host-related gene expression patterns in nematode-trapping fungi. BMC Genomics 15:968. doi:10.1186/1471-2164-15-968

    Article  Google Scholar 

  • Araujo (1998) Predacious activity of Arthrobotrys spp isolates on infective Cooperia punctata larvae. Braz J Vet Res Anim Sci 35(1):9–11

    Article  Google Scholar 

  • Ballou ER, Kozubowski L, Nichols CB, Alspaugh JA (2013) Ras1 acts through duplicated Cdc42 and Rac proteins to regulate morphogenesis and pathogenesis in the human fungal pathogen Cryptococcus neoformans. PLoS Genet 9(8):e1003687. doi:10.1371/journal.pgen.1003687

    Article  CAS  Google Scholar 

  • Banuett F, Quintanilla RH Jr, Reynaga-Pena CG (2008) The machinery for cell polarity, cell morphogenesis, and the cytoskeleton in the Basidiomycete fungus Ustilago maydis-a survey of the genome sequence. Fungal Genet Biol 45(Suppl 1):S3–S14. doi:10.1016/j.fgb.2008.05.012

    Article  CAS  Google Scholar 

  • Beck J, Ebel F (2013) Characterization of the major Woronin body protein HexA of the human pathogenic mold Aspergillus fumigatus. Int J Med Microbiol 303(2):90–97. doi:10.1016/j.ijmm.2012.11.005

    Article  CAS  Google Scholar 

  • Berepiki A, Lichius A, Read ND (2011) Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9(12):876–887. doi:10.1038/nrmicro2666

    Article  CAS  Google Scholar 

  • Braga FR, Araújo JV, Soares FE, Geniêr HL, Queiroz JH (2012) An extracellular serine protease of an isolate of Duddingtonia flagrans nematophagous fungus. Biocontrol Sci Technol 22(10):1131–1142

    Article  Google Scholar 

  • Braga FR, Carvalho RO, Silva AR, Araujo JV, Frassy LN, Lafisca A, Soares FE (2014) Predatory capability of the nematophagous fungus Arthrobotrys robusta preserved in silica gel on infecting larvae of Haemonchus contortus. Trop Anim Health Prod 46(3):571–574. doi:10.1007/s11250-014-0544-2

    Article  Google Scholar 

  • Brown AJ, Haynes K, Quinn J (2009) Nitrosative and oxidative stress responses in fungal pathogenicity. Curr Opin Microbiol 12(4):384–391. doi:10.1016/j.mib.2009.06.007

    Article  CAS  Google Scholar 

  • Cairns T, Minuzzi F, Bignell E (2010) The host-infecting fungal transcriptome. FEMS Microbiol Lett 307(1):1–11. doi:10.1111/j.1574-6968.2010.01961.x

    Article  CAS  Google Scholar 

  • Catlett NL, Yoder OC, Turgeon BG (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2(6):1151–1161

    Article  CAS  Google Scholar 

  • Chantasingh D, Kitikhun S, Keyhani NO, Boonyapakron K, Thoetkiattikul H, Pootanakit K, Eurwilaichitr L (2013) Identification of catalase as an early up-regulated gene in Beauveria bassiana and its role in entomopathogenic fungal virulence. Biol Control 67(2):85–93

    Article  CAS  Google Scholar 

  • Chen YL, Gao Y, Zhang KQ, Zou CG (2013) Autophagy is required for trap formation in the nematodet-rapping fungus Arthrobotrys oligospora. Environ Microbiol Rep 5(4):511–517. doi:10.1111/1758-2229.12054

    Article  Google Scholar 

  • Coscarelli W, Pramer D (1962) Nutrition and growth of Arthrobotrys conoides. J Bacteriol 84:60–64

    CAS  Google Scholar 

  • Cruz DG, Costa LM, Rocha LO, Retamal CA, Vieira RA, Seabra SH, Silva CP, DaMatta RA, Santos CP (2015) Serine proteases activity is important for the interaction of nematophagous fungus Duddingtonia flagrans with infective larvae of trichostrongylides and free-living nematodes Panagrellus spp. Fungal Biol 119(8):672–678.

    Article  CAS  Google Scholar 

  • Davies (2005) Interactions between nematodes and microorganisms: bridging ecological and molecular approaches. Adv Appl Microbiol 57:53–78

    Article  CAS  Google Scholar 

  • Degenkolb T, Vilcinskas A (2016a) Metabolites from nematophagous fungi and nematicidal natural products from fungi as alternatives for biological control. Part II: metabolites from nematophagous basidiomycetes and non-nematophagous fungi. Appl Microbiol Biotechnol 100(9):3813–3824. doi:10.1007/s00253-015-7234-5

    Article  CAS  Google Scholar 

  • Degenkolb T, Vilcinskas A (2016b) Metabolites from nematophagous fungi and nematicidal natural products from fungi as an alternative for biological control. Part I: metabolites from nematophagous ascomycetes. Appl Microbiol Biotechnol 100(9):3799–3812. doi:10.1007/s00253-015-7233-6

    Article  CAS  Google Scholar 

  • Dowsett JA, Reid L, Caeseele V (1977) Transmission and scanning electron microscope observations on the trapping of nematodes by Dactylaria brochopaga. Can J Bot 55(23):2945–2955

    Article  Google Scholar 

  • Drechsler (1937) Some hyphomycetes that prey on free-living terricolous nematodes. Mycologia 29(4):447–552

    Article  Google Scholar 

  • Drechsler (1941) Some hyphomycetes parasitic on free-living terriculous nematodes. Phytopathology 31(9):773–802.

    Google Scholar 

  • Duddington C (1949) A new predacious species of Trichothecium. Trans Br Mycol Soc 32(3):284–287

    Article  Google Scholar 

  • Falbo MK, Soccol VT, Sandini IE, Vicente VA, Robl D, Soccol CR (2013) Isolation and characterization of the nematophagous fungus Arthrobotrys conoides. Parasitol Res 112(1):177–185. doi:10.1007/s00436-012-3123-3

    Article  Google Scholar 

  • Fortwendel JR (2015) Orchestration of morphogenesis in filamentous fungi: conserved roles for Ras signaling networks. Fungal Biol Rev 29(2):54–62. doi:10.1016/j.fbr.2015.04.003

    Article  Google Scholar 

  • Gan Z, Yang J, Tao N, Liang L, Mi Q, Li J, Zhang KQ (2007) Cloning of the gene Lecanicillium psalliotae chitinase Lpchi1 and identification of its potential role in the biocontrol of root-knot nematode Meloidogyne incognita. Appl Microbiol Biotechnol 76(6):1309–1317. doi:10.1007/s00253-007-1111-9

    Article  CAS  Google Scholar 

  • Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36(10):3420–3435. doi:10.1093/nar/gkn176

    Article  CAS  Google Scholar 

  • Grant CL, Coscarelli W, Pramer D (1962) Statistical measurement of biotin, thiamine, and zinc concentrations required for maximal growth of Arthrobotrys conoides. Appl Microbiol 10:413–417

    CAS  Google Scholar 

  • Gronvold 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(1–4):311–325

    Article  CAS  Google Scholar 

  • Gustin MC, Albertyn J, Alexander M, Davenport K (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62(4):1264–1300

    CAS  Google Scholar 

  • Heintz CE, Pramer D (1972) Ultrastructure of nematode-trapping fungi. J Bacteriol 110(3):1163–1170

    CAS  Google Scholar 

  • Hertzberg H, Larsen M, Maurer V (2001) Biological control of helminths in grazing animals using nematophagous fungi. Berl Munch Tierarztl Wochenschr 115(7–8):278–285

    Google Scholar 

  • Hsueh YP, Mahanti P, Schroeder FC, Sternberg PW (2013) Nematode-trapping fungi eavesdrop on nematode pheromones. Curr Biol 23(1):83–86. doi:10.1016/j.cub.2012.11.035

    Article  CAS  Google Scholar 

  • Kalele DN, Affokpon A, Coosemans J, Kimenju JW (2010) Suppression of root-knot nematodes in tomato and cucumber using biological control agents. Afr J Hortic Sci 3:72–80

    Google Scholar 

  • Khan A, Williams KL, Nevalainen HK (2004) Effects of Paecilomyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biol Control 31(3):346–352

    Article  CAS  Google Scholar 

  • Khan A, Williams KL, Soon J, Nevalainen HK (2008) Proteomic analysis of the knob-producing nematode-trapping fungus Monacrosporium lysipagum. Mycol Res 112(12):1447–1452. doi:10.1016/j.mycres.2008.06.003

    Article  CAS  Google Scholar 

  • Kroll K, Pahtz V, Kniemeyer O (2013) Elucidating the fungal stress response by proteomics. J Proteom 97(31):151–163. doi:10.1016/j.jprot.2013.06.001

    Google Scholar 

  • Larriba E, Jaime MD, Carbonell-Caballero J, Conesa A, Dopazo J, Nislow C, Martin-Nieto J, Lopez-Llorca LV (2014) Sequencing and functional analysis of the genome of a nematode egg-parasitic fungus, Pochonia chlamydosporia. Fungal Genet Biol 65:69–80. doi:10.1016/j.fgb.2014.02.002

    Article  CAS  Google Scholar 

  • Lengeler KB, Davidson RC, D’Souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M, Heitman J (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64(4):746–785

    Article  CAS  Google Scholar 

  • Li J, Zou C, Xu J, Ji X, Niu X, Yang J, Huang X, Zhang KQ (2015) Molecular mechanisms of nematode-nematophagous microbe interactions: basis for biological control of plant-parasitic nematodes. Ann Rev Phytopathol 53:67–95. doi:10.1146/annurev-phyto-080614-120336

    Article  CAS  Google Scholar 

  • Liang L, Wu H, Liu Z, Shen R, Gao H, Yang J, Zhang K (2013) Proteomic and transcriptional analyses of Arthrobotrys oligospora cell wall related proteins reveal complexity of fungal virulence against nematodes. Appl Microbiol Biotechnol 97(19):8683–8692. doi:10.1007/s00253-013-5178-1

    Article  CAS  Google Scholar 

  • 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. doi:10.1186/1471-2164-15-114

    Article  Google Scholar 

  • Lorenz MC, Fink GR (2001) The glyoxylate cycle is required for fungal virulence. Nature 412(6842):83–86

    Article  CAS  Google Scholar 

  • Meerupati T, Andersson KM, Friman E, Kumar D, Tunlid A, Ahren D (2013) Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLoS Genet 9(11):e1003909. doi:10.1371/journal.pgen.1003909

    Article  Google Scholar 

  • Missall TA, Lodge JK (2005) Thioredoxin reductase is essential for viability in the fungal pathogen Cryptococcus neoformans. Eukaryot Cell 4(2):487–489. doi:10.1128/EC.4.2.487-489.2005

    Article  CAS  Google Scholar 

  • Morton OC, Hirsch PR, Kerry BR (2004) Infection of plant-parasitic nematodes by nematophagous fungi – a review of the application of molecular biology to understand infection processes and to improve biological control. Nematology 6(2):161–170

    Article  CAS  Google Scholar 

  • Nagee A, Acharya A, Shete A, Mukhopadhyaya PN, Aich BA (2008) Molecular characterization of an expressed sequence tag representing the cuticle-degrading serine protease gene (PII) from the nematophagous fungus Arthrobotrys oviformis by differential display technology. Genet Mol Res 7(4):1200–1208

    Article  CAS  Google Scholar 

  • Nguyen NV, Kim YJ, Oh KT, Jung WJ, Park RD (2008) Antifungal activity of chitinases from Trichoderma aureoviride DY-59 and Rhizopus microsporus VS-9. Curr Microbiol 56(1):28–32. doi:10.1007/s00284-007-9033-4

    Article  Google Scholar 

  • Niu XM, Zhang KQ (2011) Arthrobotrys oligospora: a model organism for understanding the interaction between fungi and nematodes. Mycology 2(2):59–78. doi:10.1080/21501203.2011.562559

    Article  CAS  Google Scholar 

  • Oka Y, Koltai H, Bar-Eyal M, Mor M, Sharon E, Chet I, Spiegel Y (2000) New strategies for the control of plant-parasitic nematodes. Pest Manag Sci 56:983–988

    Article  CAS  Google Scholar 

  • Pandit RJ, Bhatt VD, Mukhopadhyaya PN, Joshi CG, P. KA (2014a) Biochemical and molecular characterization of protease from Arthrobotrys conoides and Duddingtonia flagrans. Int J Adv Biotec Res 5(3):552–561

    CAS  Google Scholar 

  • Pandit RJ, Kunjadia PD, Mukhopadhyaya PN, Joshi CG, H. NA (2014b) Isolation, molecular characterization and predatory activity of two Indian isolates of nematode-trapping fungi. Appl Biol Res 16(1):1–11. doi:10.5958/0974-4517.2014.00042.1

    Article  Google Scholar 

  • Paris S, Wysong D, Debeaupuis JP, Shibuya K, Philippe B, Diamond RD, Latge JP (2003) Catalases of Aspergillus fumigatus. Infect Immun 71(6):3551–3562

    Article  CAS  Google Scholar 

  • Pramer D, Stoll NR (1959) Nemin: a morphogenic substance causing trap formation by predaceous fungi. Science 129(3354):966–967

    Article  CAS  Google Scholar 

  • Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11(3):R25

    Article  Google Scholar 

  • Rosen S, Ek B, Rask L, Tunlid A (1992) Purification and characterization of a surface lectin from the nematode-trapping fungus Arthrobotrys oligospora. J Gen Microbiol 138(12):2663–2672

    Article  CAS  Google Scholar 

  • Saxena G et al (1987) Interaction of nematodes with nematophagus fungi: induction of trap formation, attraction and detection of attractants. FEMS Microbiol Lett 45(6):319–327

    Article  Google Scholar 

  • Schmidt AR, Dorfelt H, Perrichot V (2007) Carnivorous fungi from Cretaceous amber. Science 318(5857):1743. doi:10.1126/science.1149947

    Article  CAS  Google Scholar 

  • Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27(6):863–864. doi:10.1093/bioinformatics/btr026

    Article  CAS  Google Scholar 

  • Shen B, Xiao J, Dai L, Huang Y, Mao Z, Lin R, Yao Y, Xie B (2015) Development of a high-efficiency gene knockout system for Pochonia chlamydosporia. Microbiol Res 170:18–26. doi:10.1016/j.micres.2014.10.001

    Article  CAS  Google Scholar 

  • Soundararajan S, Jedd G, Li X, Ramos-Pamplona M, Chua NH, Naqvi NI (2004) Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 16(6):1564–1574. doi:10.1105/tpc.020677

    Article  CAS  Google Scholar 

  • Thon M, Al-Abdallah Q, Hortschansky P, Brakhage AA (2007) The thioredoxin system of the filamentous fungus Aspergillus nidulans: impact on development and oxidative stress response. J Biol Chem 282(37):27259–27269. doi:10.1074/jbc.M704298200

    Article  Google Scholar 

  • Tikhonov VE, Lopez-Llorca LV, Salinas J, Jansson HB (2002) Purification and characterization of chitinases from the nematophagous fungi Verticillium chlamydosporium and V. suchlasporium. Fungal Genet Biol 35(1):67–78. doi:10.1006/fgbi.2001.1312

    Article  CAS  Google Scholar 

  • Tunlid A, Ahren D (2011) Molecular mechanisms of the interaction between nematode-trapping fungi and nematodes: lessons from genomics. Prog Biol Control 11:145–169. doi:10.1007/978-1-4020-9648-8_6

    Google Scholar 

  • Van Nguyen N, Kim Y-J, Oh K-T, Jung W-J, Park R-D (2007) The role of chitinase from Lecanicillium antillanum B-3 in parasitism to root-knot nematode Meloidogyne incognita eggs. Biocontrol Sci Technol 17(10):1047–1058

    Article  Google Scholar 

  • 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. Antonie Van Leeuwenhoek 56(3):251–261

    Article  CAS  Google Scholar 

  • Wang B, Liu X, Wu W, Li S (2009) Purification, characterization, and gene cloning of an alkaline serine protease from a highly virulent strain of the nematode-endoparasitic fungus Hirsutella rhossiliensis. Microbiol Res 164(6):665–673. doi:10.1016/j.micres.2009.01.003

    Article  CAS  Google Scholar 

  • Wang Y, Coleman-Derr D, Chen G, Gu YQ (2015) OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 43(W1):W78–W84. doi:10.1093/nar/gkv487

    Google Scholar 

  • Westphal A (2011) Sustainable approaches to the management of plant-parasitic nematodes and disease complexes. J Nematol 43(2):122–125

    Google Scholar 

  • Yang J, Huang X, Tian B, Wang M, Niu Q, Zhang K (2005) Isolation and characterization of a serine protease from the nematophagous fungus, Lecanicillium psalliotae, displaying nematicidal activity. Biotechnol Lett 27(15):1123–1128. doi:10.1007/s10529-005-8461-0

    Article  CAS  Google Scholar 

  • Yang J, Li J, Liang L, Tian B, Zhang Y, Cheng C, Zhang KQ (2007a) Cloning and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys conoides. Arch Microbiol 188(2):167–174. doi:10.1007/s00203-007-0233-x

    Article  CAS  Google Scholar 

  • Yang J, Liang L, Zhang Y, Li J, Zhang L, Ye F, Gan Z, Zhang KQ (2007b) Purification and cloning of a novel serine protease from the nematode-trapping fungus Dactylellina varietas and its potential roles in infection against nematodes. Appl Microbiol Biotechnol 75(3):557–565. doi:10.1007/s00253-007-0839-6

    Article  CAS  Google Scholar 

  • Yang J, Tian B, Liang L, Zhang KQ (2007c) Extracellular enzymes and the pathogenesis of nematophagous fungi. Appl Microbiol Biotechnol 75(1):21–31. doi:10.1007/s00253-007-0881-4

    Article  CAS  Google Scholar 

  • Yang Y, Yang E, An Z, Liu X (2007d) Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proc Natl Acad Sci USA 104(20):8379–8384. doi:10.1073/pnas.0702770104

    Article  CAS  Google Scholar 

  • Yang J, Gan Z, Lou Z, Tao N, Mi Q, Liang L, Sun Y, Guo Y, Huang X, Zou C, Rao Z, Meng Z, Zhang KQ (2010) Crystal structure and mutagenesis analysis of chitinase CrChi1 from the nematophagous fungus Clonostachys rosea in complex with the inhibitor caffeine. Microbiology 156(12):3566–3574. doi:10.1099/mic.0.043653-0

    Article  CAS  Google Scholar 

  • Yang J et al (2011a) Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PloS Pathog 7:e1002179. doi:10.1371/journal.ppat.1002179

    Article  CAS  Google Scholar 

  • 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, Li L, Qiao M, Feng L, Zhang KQ (2011b) Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathog 7(9):e1002179. doi:10.1371/journal.ppat.1002179

    Article  CAS  Google Scholar 

  • Yang J, Zhao X, Liang L, Xia Z, Lei L, Niu X, Zou C, Zhang KQ (2011c) Overexpression of a cuticle-degrading protease Ver112 increases the nematicidal activity of Paecilomyces lilacinus. Appl Microbiol Biotechnol 89(6):1895–1903. doi:10.1007/s00253-010-3012-6

    Article  CAS  Google Scholar 

  • You FM, Huo N, Gu YQ, Luo MC, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics 9:253. doi:10.1186/1471-2105-9-253

    Article  Google Scholar 

  • 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. Appl Microbiol Biotechnol 98(6):2555–2563. doi:10.1007/s00253-013-5432-6

    Article  CAS  Google Scholar 

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Funding

This study was funded by Gujarat State Biotechnology Mission (GSBTM), grant ID: GSBTM/MD/PROJECTS/SSA/3434/2012-13, Gandhinagar, Gujarat, India.

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Authors and Affiliations

  1. Center for Interdisciplinary Studies in Science and Technology, Sardar Patel University, New V.V. Nagar, Anand, 388 121, Gujarat, India

    Reena Patel & Anju Kunjadia

  2. Department of Animal Biotechnology, College of Veterinary Science and A.H., Anand Agricultural University, Anand, 388 001, Gujarat, India

    Ramesh Pandit, Namrata Patel & Chaitanya Joshi

  3. Department of Pharmaceutical Sciences, Saurashtra University, Rajkot, 360 005, Gujarat, India

    Vaibhav Bhatt

  4. Value Addition Research and Development Department-Human Health, National Innovation Foundation (NIF)-India, Mahudi Road, Ganhdinagar, 382650, Gujarat, India

    Pawan Kumar Singh

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  1. Ramesh Pandit
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Pandit, R., Patel, R., Patel, N. et al. RNA-Seq reveals the molecular mechanism of trapping and killing of root-knot nematodes by nematode-trapping fungi . World J Microbiol Biotechnol 33, 65 (2017). https://doi.org/10.1007/s11274-017-2232-7

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