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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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
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
Ariyawansa HA, Jaklitsch WM, Voglmayr H (2018a) Additions to Taiwan fungal flora 1: Neomassariaceae fam. Nov. Cryptogam Mycol 39(3):359–373
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
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
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
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
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
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
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
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
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
Chen Q, Hou LW, Duan WJ, Crous PW, Cai L (2017) Didymellaceae revisited. Stud Mycol 87:105–159
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
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
Dutta TK, Ganguly AK, Gaur HS (2012) Global status of rice root-knot nematode, Meloidogyne graminicola. Afr J Microbiol Res 6:6016–6021
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
Gams W, Stielow B, Grafenhan T, Schroers HJ (2019) The ascomycete genus Niesslia and associated monocillium-like anamorphs. Mycol Prog 18:5–76
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
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
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
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
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
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
Ke YH, Ju YM (2015) Two rare ophiocordycipitaceous fungi newly recorded in Taiwan. Bot Stud 56(1):30
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
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
Khan A, Williams KL, Nevalainen HKM (2006) Infection of plant-parasitic nematodes by Paecilomyces lilacinus and Monacrosporium lysipagum. BioControl 51:659–678
Kiewnick S, Sikora RA (2006) Biological control of the root-knot nematode Meloidogyne incognita by Paecilomyces lilacinus strain 251. Biol Control 38:179–187
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
Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808
Liu XZ, Xiang MC, Che YS (2009) The living strategy of nematophagous fungi. Mycoscience 50:20–25
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
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
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
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
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
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
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
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
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574
Rouxel T, Balesdent MH (2005) The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol Plant Pathol 6(3):225–241
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
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
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
Solovyev AV (2017) Limacodid moths (Lepidoptera, Limacodidae) of Taiwan, with descriptions of six new species. Entomol Rev 97(8):1140–1148
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313
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
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
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
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
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
Van Bezooijen J (2006a) Methods and techniques for nematology. Wageningen University, Wageningen, p 20
Van Bezooijen J (2006b) Methods and techniques for nematology (p. 20). Wageningen University, Wageningen, The Netherlands
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
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
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
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)
Xiao YP, Wen TC, Hyde KD (2018) Multigene phylogenetics of Polycephalomyces (Ophiocordycipitaceae, Hypocreales), with two new species from Thailand. Sci Rep 8:1
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
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
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
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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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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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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DOI: https://doi.org/10.1007/s11557-019-01546-7