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Five new species of Moelleriella infecting scale insects (Coccidae) in Thailand

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Abstract

The genus Moelleriella mostly occur on scale insects and whiteflies. It is characterized by producing brightly colored stromata, obpyriform to subglobose perithecia, cylindrical asci, disarticulating ascospores inside the ascus, and fusiform conidia, predominantly found in tropical and occasionally subtropical regions. Scale insects and whiteflies’ pathogens were found during our surveys and collections of entomopathogenic fungi. Investigations of morphological characters and multi-locus phylogenetic analyses based on partial sequences of LSU, TEF, and RPB1 were made. Five new species of Moelleriella are described here, including M. chiangmaiensis, M. flava, M. kanchanaburiensis, M. nanensis, and M. nivea. They were found on scale insects, mostly forming flat to thin, umbonate, whitish stromata. Their anamorphic and teleomorphic states were mostly often on the same stroma, possessing obpyriform perithecia, cylindrical asci with disarticulating ascospores. Their conidiomata are widely open with several locules per stroma, containing cylindrical phialides and fusiform conidia. However, M. flava has yellow stromata with one conidioma per stroma, and M. kanchanaburiensis was found only in its anamorphic state. Furthermore, the perithecia of M. nanensis were completely embedded in stromata as opposed to other species with semi-immersed perithecia. We also found a teleomorph link to M. sinensis, a species described based on anamorphic stage previously reported from southeastern China.

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Data availability

All sequence data generated in this study (see Table 1) are available in GenBank (https://www.ncbi.nlm.nih.gov/genbank/).

References

  • Chaverri P, Bischoff JF, Evan HC, Hodge KT (2005a) Regiocrella, a new entomopathogenic genus with a pycnidial anamorph and its phylogenetic placement in the Clavicipitaceae. Mycologia 97(6):1225–1237. https://doi.org/10.3852/mycologia.97.6.1225

    Article  PubMed  Google Scholar 

  • Chaverri P, Bischoff JF, Hodge KT (2005b) A new species of Hypocrella, H. macrostroma, and its relationship to other species with large stromata. Mycol Res 109:126–1275. https://doi.org/10.1017/S0953756205003904

    Article  Google Scholar 

  • Chaverri P, Liu M, Hodge KT (2008) A monograph of the entomopathogenic genera Hypocrella, Moelleriella and Samuelsia gen nov.(Ascomycota, Hypocreales, Clavicipitaceae) and their aschersonia-like anamorphs in the Neotropics. Stud Mycol 60:1–66. https://doi.org/10.3114/sim.2008.60.01

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen YX, Xue QL, XIE YX, Keyhani NO, Guan XY, Wei XY, Zhao J, Yan Z, Chen H, Qui JZ, Guan X (2020) Moelleriella sinensis sp. nov. (Clavicipitaceae, Ascomycota) from southeast China. Phytotaxa 429(4):289–296. https://doi.org/10.11646/phytotaxa.429.4.5

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hywel-Jones NL, Evans HC (1993) Taxonomy and ecology of Hypocrella discoidea and its anamorph, Aschersonia samoensis. Mycol Res 97:871–876. https://doi.org/10.1016/S0953-7562(09)81165-9

    Article  Google Scholar 

  • Hywel-Jones NL, Samuels GJ (1998) Three species of Hypocrella with large stromata pathogenic on scale insects. Mycologia 90:36–46. https://doi.org/10.1080/00275514.1998.12026876

    Article  Google Scholar 

  • Johnson D, Sung GH, Hywel-Jones NL, Luangsa-ard JJ, Bischoff JF, Kepler RM, Spatafora JW (2009) Systematics and evolution of the genus Torrubiella (Hypocreales, Ascomycota). Mycol Res 113:279–289. https://doi.org/10.1016/j.mycres.2008.09.008

    Article  CAS  PubMed  Google Scholar 

  • Khonsanit A, Luangsa-ard JJ, Thanakitpipattana D, Noisripoom W, Chaitika T, Kobmoo N (2020) Cryptic diversity of the genus Beauveria with a new species from Thailand. Mycol Prog 19:291–315. https://doi.org/10.1007/s11557-020-01557-9

    Article  Google Scholar 

  • Li GJ, Hyde KD, Zhao RL, Hongsanan S, Abdel-Aziz FA, Abdel-Wahab MA, Alvarado P, Alves-Silva G, Ammirati JF, Ariyawansa HA, Baghela A, Bahkali AH, Beug M, Bhat DJ, Bojantchev D, Boonpratuang T, Bulgakov TS, Camporesi E, Boro MC, Ceska O, Chakraborty D, Chen JJ, Chethana KWT, Chomnunti P, Consiglio G, Cui BK, Dai DQ, Dai YC, Dinushani A, Daranagama DA, Das K, Dayarathne MC, Crop ED, De Oliveira RJV, Fragoso de Souza CA, de Souza JI, Dentinger BTM, Dissanayake AJ, Mingkwan D, Drechsler-Santos ER, Ghobad-Nejhad M, Gilmore SP, Góes-Neto A, Gorczak M, Haitjema CH, Hapuarachchi KK, Akira Hashimoto A, He MQ, Henske JK, Hirayama K, Iribarren MJ, Jayasiri SC, Jayawardena RS, Jeon SJ, Jerônimo GH, Jesus AL, EBG J, Kang JC, Karunarathna SC, Kirk PM, Konta S, Kuhnert E, Langer E, Lee HS, Lee HB, Li WJ, Li XH, Liimatainen K, Lima DX, Lin CG, Liu JK, Liu XZ, Liu ZY, Luangsa-ard JJ, Lücking R, Lumbsch HT, Lumyong S, Leaño EM, Marano AV, Matsumura M, McKenzie EHC, Mongkolsamrit S, Mortimer PE, TTT N, Niskanen T, Norphanphoun C, O’Malley MA, Parnmen S, Pawłowska J, Perera RH, Phookamsak R, Phukhamsakda C, Pires-Zottarelli CLA, Raspé O, Reck MA, Rocha SCO, de Azevedo Santiago Cabral Monteiro AL, Senanayake IC, Setti L, Shang QJ, Singh SK, Sir EB, Solomon KV, Song J, Srikitikulchai P, Stadler M, Suetrong S, Takahashi H, Takahashi T, Tanaka K, Tang LP, Thambugala KM, Thanakitpipattana D, Theodorou MK, Thongbai B, Thummarukcharoen T, Tian Q, Tibpromma S, Verbeken A, Vizzini A, Vlasák J, Voigt K, Wanasinghe DN, Wang Y, Weerakoon G, Wen HA, Wen TC, Wijayawardene NN, Wongkanoun S, Wrzosek M, Xiao YP, Xu JC, Yan JY, Yang J, Yang SD, Hu Y, Zhang JF, Zhao J, Zhou LW, Peršoh D, Phillips AJL, Maharachchikumbura SSN (2016) Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 78:1–237. https://doi.org/10.1007/s13225-016-0366-9

    Article  CAS  Google Scholar 

  • Liu M, Hodge KT (2005) Hypocrella zhongdongii sp. nov., the teleomorph of Aschersonia incrassa. Mycol Res 109(7):818–824. https://doi.org/10.1017/S095375620500290

    Article  PubMed  Google Scholar 

  • Liu M, Chaverri P, Hodge KT (2006) A taxonomic revision of the insect biocontrol fungus Aschersonia aleyrodis, its allies with white stromata and their Hypocrella sexual states. Mycol Res 110:537–554. https://doi.org/10.1016/j.mycres.2006.01.013

    Article  CAS  PubMed  Google Scholar 

  • Luangsa-ard JJ, Tasanathai K, Mongkolsamrit S, Hywel-Jones NL (2008) Atlas of Invertebrate -Pathogenic Fungi of Thailand Volume 2. National Center for Genetic Engineering and Biotechnology. National Science and Technology Development Agency, Pathum Thani

    Google Scholar 

  • Luangsa-ard JJ, Tasanathai K, Mongkolsamrit S, Hywel-Jones NL (2012) Atlas of Invertebrate-Pathogenic Fungi of Thailand Volume 4. National Center for Genetic Engineering and Biotechnology. National Science and Technology Development Agency, Pathum Thani

    Google Scholar 

  • Luangsa-ard JJ, Mongkolsamrit S, Noisripoom W, Thanakitpipattana D, Khonsanit A, Wutikhun T (2017) Helicocollum, a new clavicipitalean genus pathogenic to scale insects (Hemiptera) in Thailand. Mycol Res 16:419–431. https://doi.org/10.1007/s11557-017-283-3

    Article  Google Scholar 

  • Mains EB (1959a) Species of Aschersonia (Sphaeropsidales). Lloydia 22:215–221

    Google Scholar 

  • Mains EB (1959b) Species of Hypocrella. Mycopathol Mycol Appl 11:311–326

    Article  CAS  Google Scholar 

  • Mongkolsamrit S, Spatafora JW, Luangsa-ard JJ, Sung GH, Hywel-Jones NL (2009) A combined ITS rDNA and β-tubulin phylogeny of Thai species of Hypocrella with non-fragmenting ascospores. Mycol Res 113:684–699. https://doi.org/10.1016/j.mycres.2009.02.004

    Article  CAS  PubMed  Google Scholar 

  • Mongkolsamrit S, Luangsa-ard JJ, Tasanathai K, Sivichai S (2010) Invertebrate-pathogenic fungi of Thailand, National Center for Genetic Engineering and Biotechnology. National Science and Technology Development Agency, Pathum Thani

    Google Scholar 

  • Mongkolsamrit S, Luangsa-ard JJ, Hywel-Jones NL (2011a) Samuelsia mundiveteris sp. nov. from Thailand. Mycologia 103:921–927. https://doi.org/10.3852/11-049

    Article  PubMed  Google Scholar 

  • Mongkolsamrit S, Nguyen TT, Tran NL, Luangsa-ard JJ (2011b) Moelleriella pumatensis, new entomogenous species from Vietnam. Mycotaxon 117:45–51. https://doi.org/10.5248/117.45

    Article  Google Scholar 

  • Mongkolsamrit S, Khonsanit A, Noisripoom W, Luangsa-ard JJ (2015) Two new entomogenous species of Moelleriella with perithecia in tubercles from Thailand. Mycoscience 56:66–74. https://doi.org/10.1016/j.myc.2014.03.002

    Article  Google Scholar 

  • Mongkolsamrit S, Noisripoom W, Thanakitpipattana D, Wutikhun T, Spatafora JW, Luangsa-ard JJ (2018) Disentangling cryptic species with isaria-like morphs in Cordycipitaceae. Mycologia 110:230–257. https://doi.org/10.1080/00275514.2018.1446651

    Article  PubMed  Google Scholar 

  • Montagne JPFC (1848) Sixie`me centurie de plantes cellulaires exotiques nouvelles. Crypto gamae Taitenses. Ann des Sci Nat Bota Série 3(10):106–136

    Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary biology Centre, Uppsala University

  • Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Petch T (1921) Studies in entomogenous fungi. II The genera of Hypocrella and Aschersonia. Ann Roy Bot Gard (Peradeniya) 7:167–278

    Google Scholar 

  • Petch T (1925) Entomogenous fungi. Addition and corrections. Trans Br Mycol Soc 10:190–201

    Article  Google Scholar 

  • Petch T (1931) Note on entomogenous fungi, 22-48. Trans Br Mycol Soc 16:55–75

    Article  Google Scholar 

  • Petch T (1932) Notes on entomogenous fungi. Trans Br Mycol Soc 16:209–245

    Article  Google Scholar 

  • Qiu JZ, Guan X (2010) A new species of Aschersonia (Clavicipitaceae, Hypocreales) from China. Mycotaxon 111:471–475. https://doi.org/10.5248/111.471

    Article  Google Scholar 

  • Qiu JZ, Ma HF, Wang YY, Guan X (2009) Two Aschersonia species from Fujian new to China. Mycosystema 28:60–63

    Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • Saccardo PA (1878) Enumeratio pyrenomycetum hypocreaceorum. Michelia 1:277–325

    Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.3114/sim.2007.57.01

    Article  PubMed  PubMed Central  Google Scholar 

  • Tadych M, Chaverri P, Bergen M, White JF (2009) Moelleriella zhongdongii: stroma development and identification of hirsutella-like and Aschersonia synanamorphs. Mycol Res 113(5):611–615. https://doi.org/10.1016/j.mycres.2009.01.011

    Article  PubMed  PubMed Central  Google Scholar 

  • The Royal Horticultural Society (2007) The Fifth Edition Published by The Royal Horticultural Society. Vincent Square, London

    Google Scholar 

  • Tibpromma S, Hyde KD, Jeewon R, Maharachchikumbura SSN, Liu JK, Bhat DJ, Jones EBG, McKenzie EHC, Camporesi E, Bulgakov TS, Doilom M, de Azevedo Santiago Cabral Monteiro AL, Das K, Manimohan P, Gibertoni TB, Lim YW, Ekanayaka AH, Thongbai B, Lee HB, Yang JB, Kirk PM, Sysouphanthong P, Singh SK, Boonmee S, Dong W, Raj KNA, Latha KP, Phookamsak R, Phukhamsakda C, Konta S, Jayasiri SC, Norphanphoun C, Tennakoon DS, Li J, Dayarathne MC, Perera RH, Xiao Y, Wanasinghe DN, Senanayake IC, Goonasekara ID, de Silva NI, Mapook A, Jayawardena RS, Dissanayake AJ, Manawasinghe IS, Chethana KWT, Luo ZL, Hapuarachchi KK, Baghela A, Soares AM, Vizzini A, Meiras-Ottoni A, Mešic A, Dutta AK, Fragoso de Souza CA, Richter C, Lin CG, Chakrabarty D, Daranagama DA, Lima DX (2017) Fungal diversity notes 491–602: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 83:1–261. https://doi.org/10.1007/s13225-017-0378-0

    Article  Google Scholar 

  • Yuan HS, Lu X, Dai YC, Hyde KD, Kan YH, Kusan I, He SH, Liu NG, Sarma VV, Zhao CL, Cui BK, Yousaf N, Sun G, Liu SY, Wu F, Lin CG, Dayarathne MC, Gibertoni TB, Conceição LB, Garibay-Oriejel R, Villegas-Ríos M, Salas-Lizana R, Wei TZ, Qiu JZ, Yu ZF, Phookamsak R, Zeng M, Paloi S, Bao DF, Abeywickrama PD, Wei DP, Yang J, Manawasinghe IS, Harishchandra D, Brahmanage RS, de Silva NI, Tennakoon DS, Karunarathna A, Gafforov Y, Pem D, Zhang SN, de Azevedo Santiago Cabral Monteiro AL, Bezerra JDP, Dima B, Acharya K, Alvarez-Manjarrez J, Ali H, Bahkali AH, Bhatt VK, Brandrud TE, Bulgakov TS, Camporesi E, Cao T, Chen YX, Chen YY, Devadatha B, Elgorban AM, Fan LF, Du X, Gao L, Gonçalves CM, Gusmão LFP, Huanraluek N, Jadan M, Jayawardena RS, Khalid AN, Langer E, Lima DX, de Lima-Júnior NC, de Lira CRS, Liu JK, Liu S, Lumyong S, Luo ZL, Matoçec N, Niranjan M, Oliveira-Filho JRC, Papp V, Pérez-Pazon E, Phillips AJL, Qui PL, Ren Y, Ruiz RFC, Semwal KC, Soop K, de Souza CAF, Souza-Motta CM, Sun LH, Xie ML, Yao YJ, Zhao Q, Zhou LW (2020) Fungal diversity notes 1277–1386: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 104:1–266. https://doi.org/10.1007/s13225-020-00461-7

    Article  Google Scholar 

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Acknowledgements

We gratefully acknowledge the Royal Forest Department of Thailand, Department of National Parks, Wildlife and Plant Conservation of Thailand (DNP), for permission to survey and collect insect fungi in national parks and wildlife sanctuaries. We thank the staff of Plant Microbe Interaction Research Team (APMT members; Boonchan Thongnuch, Donnaya Thanakitpipattana, Jiranan Techaprasarn, Kanoksri Tasanathai, and Rachada Promharn) for collecting samples and providing specimens and cultures. We also thank Dr. Noppol Kobmoo for editing the manuscript.

Funding

This study was supported by the National Center for Genetic Engineering and Biotechnology (BIOTEC) Platform Technology Management (Grant no. P19-50231)

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The samples in this study were collected by A. Khonsanit, J.J. Luangsa-ard, S. Mongkolsamrit, W. Noisripoom, and APMT members. Mophological investigations were observed and illustrated by A. Khonsanit. The insect hosts were identified by N. Phosrithong. Description of the new and known species were described by A. Khonsanit and S. Mongkolsamrit. Molecular data and phylogenetic analyses were performed by W. Noisripoom. A. Khonsanit and S. Mongkolsamrit wrote the original draft, and review and editing were performed by A. Khonsanit, S. Mongkolsamrit, and J.J. Luangsa-ard. All authors have read and approved the manuscript.

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Correspondence to Janet Jennifer Luangsa-ard.

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Khonsanit, A., Noisripoom, W., Mongkolsamrit, S. et al. Five new species of Moelleriella infecting scale insects (Coccidae) in Thailand. Mycol Progress 20, 847–867 (2021). https://doi.org/10.1007/s11557-021-01709-5

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