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In vitro inferred interactions of selected entomopathogenic fungi from Taiwan and eggs of Meloidogyne graminicola

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Abstract

Nematophagous fungi, mostly belonging to the phylum Ascomycota, have raised great attention because of their potential use against plant-pathogenic nematodes. In this investigation, entomopathogenic fungi were collected in Taiwan and isolated and identified based on molecular phylogenetic analyses of six nuclear loci including LSU, ITS, TEF1, RPB1, RPB2, and TUB2 combined with morphological data. Two novel fungal taxa are described in the present study, namely, Paraboeremia taiwanensis (Pleosporales) and Polycephalomyces elaphomyceticola (Hypocreales), respectively. Both species showed the ability to parasitize eggs of the rice root-knot nematode, Meloidogyne graminicola, in in vitro assays. Size ranges of conidiomata and conidia distinguish Paraboeremia taiwanensis from other currently known Paraboeremia species. Polycephalomyces elaphomyceticola differs from other Polycephalomyces species by producing single stromata, smaller perithecia, awl-shaped phialides, and monomorphic conidia. It was encountered as a parasite on Elaphomyces muricatus. Both examined strains grew and sporulated well on artificial media. Pathogenicity testing showed that they were capable of parasitizing eggs of Meloidogyne graminicola. In addition, our study elucidated the teleomorph of Polycephalomyces agaricus for the first time.

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References

  • Ariyawansa HA, Tanaka K, Thambugala KM, Bulgakov TS, Wanasinghe DN, Perera RH, Mapook A, Chukeatirote E, Kang JC, Xu JC, McKenzie EHC, Gareth Jones EB, Hyde KD (2014) A molecular phylogenetic reappraisal of the Didymosphaeriaceae (= Montagnulaceae). Fungal Divers 68:69–104

    Article  Google Scholar 

  • Ariyawansa HA, Phukhamsakda C, Thambugala KM, Bulgakov TS, Wanasinghe DN, Perera RH, Mapook A, Camporesi E, Kang JC, Gareth Jones EB, Bahkali AH, Jayasiri SC, Hyde KD, Bhat JD (2015) Revision and phylogeny of Leptosphaeriaceae. Fungal Divers 74:19–51

    Article  Google Scholar 

  • Ariyawansa HA, Jaklitsch WM, Voglmayr H (2018a) Additions to Taiwan fungal flora 1: Neomassariaceae fam. Nov. Cryptogam Mycol 39(3):359–373

    Article  Google Scholar 

  • Ariyawansa HA, Phillips AJL, Chuang WY, Tsai I (2018b) Tzeananiaceae, a new pleosporalean family associated with Ophiocordyceps macroacicularis fruiting bodies in Taiwan. MycoKeys 37:1–17

    Article  Google Scholar 

  • Ashrafi S, Helaly S, Schroers HJ, Stadler M, Richert-Poeggeler KR, Dababat AA, Maier W (2017) Ijuhya vitellina sp. nov., a novel source for chaetoglobosin a, is a destructive parasite of the cereal cyst nematode Heterodera filipjevi. PLoS One 12:e0180032

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aveskamp MM, De Gruyter J, Woudenberg JHC, Verkley GJM, Crous PW (2010) Highlights of the Didymellaceae: a polyphasic approach to characterise Phoma and related pleosporalean genera. Stud Mycol 65:1–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ban S, Sakane T, Toyama K, Nakagiri A (2009) Teleomorph–anamorph relationships and reclassification of Cordyceps cuboidea and its allied species. Mycoscience 50:261–272

    Article  Google Scholar 

  • Baral HO, Weber E, Gams W, Hadedorn G, Liu B, Liu X, Marvanová L, Stadler M, Weiß M (2018) Generic names in the Orbiliaceae (Orbiliomycetes) and recommendations on which names should be protected or suppressed. Mycol Prog 17:5–31

    Article  Google Scholar 

  • Becker JS, Borneman J, Becker JO (2013) Dactylella oviparasitica parasitism of the sugar beet cyst nematode observed in trixenic culture plates. Biol Control 64:51–56

    Article  Google Scholar 

  • Brar D, Soriano I, Reversat G, Schmit V, Prot JC (1999) Resistance to rice root-knot nematode Meloidogyne graminicola identified in Oryza longistaminata and O. glaberrima. Nematology 1:395–398

    Article  Google Scholar 

  • Bridge J, Michel L, Sikora RA (CABI, 1990) Nematode parasites of rice in plant parasitic nematodes in subtropical and tropical agriculture (eds Luc, M., Sikora, R. A. & Bridge, J.), pp 69–108

    Google Scholar 

  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia:553–556

  • Chen Q, Jiang JR, Zhang GZ, Cai L, Crous PW (2015) Resolving the Phoma enigma. Stud Mycol 82:137–217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Hou LW, Duan WJ, Crous PW, Cai L (2017) Didymellaceae revisited. Stud Mycol 87:105–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Gruyter J, Woudenberg JH, Aveskamp MM, Verkley GJ, Groenewald JZ, Crous PW (2013) Redisposition of Phoma-like anamorphs in Pleosporales. Stud Mycol 75:1–36

    Article  PubMed  Google Scholar 

  • Dimkpa SO, Lahari Z, Shrestha R, Douglas A, Gheysen G, Price AH (2015) A genome-wide association study of a global rice panel reveals resistance in Oryza sativa to root-knot nematodes. J Exp Bot 67:1191–1200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dutta TK, Ganguly AK, Gaur HS (2012) Global status of rice root-knot nematode, Meloidogyne graminicola. Afr J Microbiol Res 6:6016–6021

    Article  Google Scholar 

  • Fiedler Ż, Sosnowska D (2007) Nematophagous fungus Paecilomyces lilacinus (Thom) Samson is also a biological agent for control of greenhouse insects and mite pests. BioControl 52:547–558

    Article  Google Scholar 

  • Gams W, Stielow B, Grafenhan T, Schroers HJ (2019) The ascomycete genus Niesslia and associated monocillium-like anamorphs. Mycol Prog 18:5–76

    Article  Google Scholar 

  • Goffré D, Folgarait P (2015) Purpureocillium lilacinum, potential agent for biological control of the leaf-cutting ant Acromyrmex lundii. J Invertebr Pathol 130:107–115

    Article  PubMed  Google Scholar 

  • Helaly SE, Ashrafi S, Teponno RB, Bernecker S, Dababat AA, Maier W, Stadler M (2018) Nematicidal cyclic lipodepsipeptides and a xanthocillin derivative from a pleosporalean fungus parasitizing eggs of the plant parasitic nematode Heterodera filipjei. J Nat Prod 81:2228–2234

    Article  CAS  PubMed  Google Scholar 

  • Hernández-Restrepo M, Gené J, Castañeda-Ruiz RF, Mena-Portales J, Crous PW, Guarro J (2017) Phylogeny of saprobic microfungi from southern Europe. Stud Mycol 86:53–97

    Article  PubMed  PubMed Central  Google Scholar 

  • Hyde KD, Gareth Jones EB, Liu JK, Ariyawansa H, Boehm E, Boonmee S, Braun U, Chomnunti P, Crous PW, Dai DQ, Diederich P, Dissanayake A, Doilom M, Doveri F, Hongsanan S, Jayawardena R, Lawrey JD, Li YM, Liu YX, Lücking R, Monkai J, Muggia L, Nelsen MP, Pang KL, Phookamsak R, Senanayake IC, Shearer CA, Suetrong S, Tanaka K, Thambugala KM, Wijayawardene NN, Wikee S, Wu HX, Zhang Y, Aguirre-Hudson B, Alias SA, Aptroot A, Bahkali AH, Bezerra JL, Jayarama Bhat D, Camporesi E, Chukeatirote E, Gueidan C, Hawksworth DL, Hirayama K, De Hoog S, Kang JC, Knudsen K, Li WJ, Li XH, Liu ZY, Mapook A, McKenzie EHC, Miller AN, Mortimer PE, Phillips AJL, Raja HA, Scheuer C, Schumm F, Taylor JE, Tian Q, Tibpromma S, Wanasinghe DN, Wang Y, Xu JC, Yacharoen S, Yan JY (2013) Families of Dothideomycetes. Fungal Divers 63:1–313

    Article  Google Scholar 

  • Hyde KD, Xu JC, Rapior S, Jeewon R, Lumyong S, Niego AGT, Abeywickrama PD, Aluthmuhandiram JPS, Brahamanage RS, Brooks S, Chaiyasen A, Chethana KWT, Chomnunti P, Chepkirui K, Chuankid B, de Silva NI, Doilom M, Faulds C, Gentekaki E, Gopalan V, Kakumyan P, Harishchandra D, Hemachandran H, Hongsanan S, Karunarathna A, Karunarathna SC, Khan S, Kumla J, Jayawardena RS, Liu N, Luangharn T, Macabeo APG, Marasinghe DS, Meeks D, Mortimer PE, Mueller P, Nadir S, Nataraja KN, Nontachaiyapoom S, O’Brien M, Penkhrue W, Phukhamsakda C, Shaanker Ramanan U, Rathnayaka AR, Sadaba RS, Sandargo B, Samarakoon BC, Tennakoon DS, Siva R, Sriprom W, Suryanarayanan TS, Sujarit K, Suwannarach N, Suwunwong T, Thongbai B, Thongklang N, Wei D, Wijesinghe NS, Winiski J, Yan J, Yasanthika E, Stadler M (2019) The amazing potential of fungi, 50 ways we can exploit fungi industrially. Fungal Divers 97:1–136

    Article  Google Scholar 

  • Jamshidnejad V, Sahebani N, Etebarian H (2013) Potential biocontrol activity of Arthrobotrys oligospora and Trichoderma harzianum BI against Meloidogyne javanica on tomato in the greenhouse and laboratory studies. Arch Phytopathol Plant Protect 46:1477–2906

    Article  Google Scholar 

  • Ke YH, Ju YM (2015) Two rare ophiocordycipitaceous fungi newly recorded in Taiwan. Bot Stud 56(1):30

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kepler R, Ban S, Nakagiri A, Bischoff J, Hywel-Jones N, Owensby CA, Spatafora JW (2013) The phylogenetic placement of hypocrealean insect pathogens in the genus Polycephalomyces: an application of one fungus one name. Fungal Biol 117:611–622

    Article  PubMed  Google Scholar 

  • Kerry BR, Hirsch PR (2011) Ecology of Pochonia chlamydosporia in the rhizosphere at the population, whole organism and molecular scales. In: Davies K, Spiegel Y (eds) biological control of plant-parasitic nematodes, pp 171–182

    Chapter  Google Scholar 

  • Khan A, Williams KL, Nevalainen HKM (2006) Infection of plant-parasitic nematodes by Paecilomyces lilacinus and Monacrosporium lysipagum. BioControl 51:659–678

    Article  Google Scholar 

  • Kiewnick S, Sikora RA (2006) Biological control of the root-knot nematode Meloidogyne incognita by Paecilomyces lilacinus strain 251. Biol Control 38:179–187

    Article  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. Annu Rev Phytopathol 53:67–95

    Article  CAS  PubMed  Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808

    Article  CAS  PubMed  Google Scholar 

  • Liu XZ, Xiang MC, Che YS (2009) The living strategy of nematophagous fungi. Mycoscience 50:20–25

    Article  Google Scholar 

  • Lopez-Llorca LV, Maciá-Vicente JG, Jansson HB (2008) 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, Dordrecht

    Google Scholar 

  • Manzanilla-López RH, Manzanilla-López RH, Esteves I, Finetti-Sialer MM, Hirsch PR, Ward E, Devonshire J, Hidalgo-Díaz L (2013) Pochonia chlamydosporia: advances and challenges to improve its performance as a biological control agent of sedentary endo-parasitic nematodes. J Nematol 45(1)

  • Matočec N, Kušan I, Ozimec R (2014) The genus Polycephalomyces (Hypocreales) in the frame of monitoring Veternica cave (Croatia) with a new segregate genus Perennicordyceps. Ascomycete org 6:125–133

    Google Scholar 

  • McDonald GK, Peck D (2009) Effects of crop rotation, residue retention and sowing time on the incidence and survival of ascochyta blight and its effect on grain yield of field peas (Pisum sativum L.). Field Crop Res 111:11–21

    Article  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In gateway computing environments workshop (GCE):1–8

  • Nahar K, Kyndt T, De Vleesschauwer D, Höfte M, Gheysen G (2011) The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 157:305–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narasimhamurthy H, Ravindra H, Mukesh Sehgal RN, Suresha D (2018) Biology and life cycle of rice root-knot nematode (Meloidogyne graminicola)

  • Nordbring-Hertz B, Jansson HB, Tunlid A (2011) Nematophagous fungi. eLS (Ed.)

  • Nylander J (2004) MrModeltest v2. Program distributed by the author. Uppsala University, Uppsala, Sweden, Evolutionary Biology Centre

    Google Scholar 

  • Padgham J, Duxbury J, Mazid A, Abawi G, Hossain M (2004) Yield loss caused by Meloidogyne graminicola on lowland rainfed rice in Bangladesh. J Nematol 36:42

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pankaj SH, Prasad J (2010) The rice root-knot nematode, Meloidogyne graminicola: an emerging problem in rice-wheat cropping system. Indian J Nematol 1:1–11

    Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1, 4. http://beast.bio.ed.ac.uk/tracer

  • Rao Y, Biswas H (1974) Evaluation of yield losses in rice due to the root-knot nematode Meloidogyne incognita. Indian J Nematol 3:74

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rouxel T, Balesdent MH (2005) The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol Plant Pathol 6(3):225–241

    Article  CAS  PubMed  Google Scholar 

  • Rupcic Z, Chepkirui C, Hernández-Restrepo M, Crous PW, Luangsa-ard JJ, Stadler M (2018) New nematicidal and antimicrobial secondary metabolites from a new species in the new genus, Pseudobambusicola thailandica. MycoKeys 33:1–23

    Article  Google Scholar 

  • Salam MU, MacLeod WJ, Maling T, Prichard I, Seymour M, Barbetti MJ (2011) A meta-analysis of severity and yield loss from ascochyta blight on field pea in Western Australia. Australas Plant Pathol 40(6):591–600

    Article  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, André Levesque C, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109:6241–6246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solovyev AV (2017) Limacodid moths (Lepidoptera, Limacodidae) of Taiwan, with descriptions of six new species. Entomol Rev 97(8):1140–1148

    Article  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stielow B, Bubner B, Hensel G, Münzenberger B, Hoffmann P, Klenk HP, Göker M (2010) The neglected hypogeous fungus Hydnotrya bailii Soehner (1959) is a widespread sister taxon of Hydnotrya tulasnei (Berk.) Berk. And Broome (1846). Mycol Prog 9:195–203

    Article  Google Scholar 

  • Stirling GR (2017) Biological control of plant-parasitic nematodes. In diseases of nematodes. CRC press, pp 103–150

  • Sung GH, Hywel-Jones NL, Sung JM, Luangsa-ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57:5–59

    Article  PubMed  PubMed Central  Google Scholar 

  • Szabó M, Csepregi K, Gálber M, Virányi F, Fekete C (2012) Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: the role of chi18-5 and chi18-12 genes in nematode egg-parasitism. Biol Control 63:121–128

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valenzuela-Lopez N, Cano-Lira JF, Guarro J, Sutton DA, Wiederhold N, Crous PW, Stchigel AM (2018) Coelomycetous Dothideomycetes with emphasis on the families Cucurbitariaceae and Didymellaceae. Stud Mycol 1(90):1–69

    Article  CAS  PubMed  Google Scholar 

  • Van Bezooijen J (2006a) Methods and techniques for nematology. Wageningen University, Wageningen, p 20

    Google Scholar 

  • Van Bezooijen J (2006b) Methods and techniques for nematology (p. 20). Wageningen University, Wageningen, The Netherlands

    Google Scholar 

  • Wang YB, Yu H, Dai YD, Wu CK, Zeng WB, Yuan F, Liang Z (2015) Q. Polycephalomyces agaricus, a new hyperparasite of Ophiocordyceps sp. infecting melolonthid larvae in southwestern China. Mycol Prog 14(9):70

    Article  Google Scholar 

  • Wang N, Zhang Y, Hussain M, Li K, Xiang M, Liu X (2016) The mitochondrial genome of the nematode endoparasitic fungus Hirsutella rhossiliensis. Mitochondrial DNA Part B 1:114–115

    Article  PubMed  PubMed Central  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols 18:315–322

    Google Scholar 

  • Woo SL, Ruocco M, Vinale F, Nigro M, Marra R, Lombardi N, Pascale A, Lanzuise S, Manganiello G, Lorito M (2014) Trichoderma-based products and their widespread use in agriculture. Open Mycol J 8(1)

    Article  Google Scholar 

  • Xiao YP, Wen TC, Hyde KD (2018) Multigene phylogenetics of Polycephalomyces (Ophiocordycipitaceae, Hypocreales), with two new species from Thailand. Sci Rep 8:1

    Article  CAS  Google Scholar 

  • Yang JI, Benecke S, Jeske DR, Rocha FS, Recker JS, Timper P, Becker JO, Borneman J (2012a) Population dynamics of Dactylella oviparasitica and Heterodera schachtii: toward a decision model for sugar beet planting. J Nematol 44:237

    PubMed  PubMed Central  Google Scholar 

  • Yang JI, Loffredo A, Borneman J, Becker JO (2012b) Biocontrol efficacy among strains of Pochonia chlamydosporia obtained from a root-knot nematode suppressive soil. J Nematol 44:67

    PubMed  PubMed Central  Google Scholar 

  • Zhang S, Gan Y, Xu B, Xue Y (2014) The parasitic and lethal effects of Trichoderma longibrachiatum against Heterodera avenae. Biol Control 72:1–8

    Article  Google Scholar 

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Acknowledgments

The authors thank Dr. Wen-Jer Wu and Dr. Shiuh-Feng Shiao (Department of Entomology, NTU) for insect identification assistance and Ms. Yu-Jie Liang (Department of Plant Pathology & Microbiology) for nematode experiment assistance. Hiran Ariyawansa is grateful to A.D. Ariyawansa, D.M.K. Ariyawansa, Ruwini Ariyawansa, Amila Gunasekara, and Oshen Chemika for their valuable suggestions.

Funding

This study was funded by the Ministry of Science and Technology, Taiwan (MOST project ID: 106–2621–B–002–005–MY2).

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Authors and Affiliations

  1. Department of Plant Pathology and Microbiology, College of Bio-Resources and Agriculture, National Taiwan University, Taipei, Taiwan

    Jiue-in Yang, Wei-Yu Chuang & Hiran A. Ariyawansa

  2. Department Microbial Drugs, Helmholtz Centre for Infection Research GmbH (HZI), Braunschweig, Germany

    Marc Stadler

  3. Biodiversity Research Center, Academia Sinica, Taiwan, No.128, Sec. 2, Academia Rd., Nangang, 11529, Taipei, Taiwan

    Shipher Wu

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Contributions

H.A.A and J.Y designed the study. H.A.A, W.Y.C, and J.Y conducted all the experiments. H.A.A, W.Y.C, J.Y, M.S., and S.W. analyzed the result. H.A.A, W.Y.C, J.Y, M.S., and S.W. edited the manuscript. All authors reviewed the manuscript and approved the manuscript for publication.

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Correspondence to Hiran A. Ariyawansa.

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Yang, Ji., Stadler, M., Chuang, WY. et al. In vitro inferred interactions of selected entomopathogenic fungi from Taiwan and eggs of Meloidogyne graminicola. Mycol Progress 19, 97–109 (2020). https://doi.org/10.1007/s11557-019-01546-7

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