Bringing Laboulbeniales into the 21st century: enhanced techniques for extraction and PCR amplification of DNA from minute ectoparasitic fungi

Danny Haelewaters; Michał Gorczak; Walter P. Pfliegler; András Tartally; Marta Tischer; Marta Wrzosek; Donald H. Pfister

doi:10.5598/imafungus.2015.06.02.08

Danny Haelewaters, Walter P. Pfliegler, Tamara Szentiványi, Mihály Földvári, Attila D. Sándor, Levente Barti, Jasmin J. Camacho, Gerrit Gort, Péter Estók, Thomas Hiller, Carl W. Dick, Donald H. Pfister (2017)
Parasites of parasites of bats: Laboulbeniales (Fungi: Ascomycota) on bat flies (Diptera: Nycteribiidae) in central Europe. Parasites & Vectors 10: .

DOI: 10.1186/s13071-017-2022-y

Warre Van Caenegem, Aimée Blondelle, Iris Dumolein, Brianna Santamaria, Carl W. Dick, Thomas Hiller, Jingyu Liu, C. Alisha Quandt, Rosa V. Villarreal Saucedo, Annemieke Verbeken, Danny Haelewaters (2023)
Five new species of Gloeandromyces (Fungi, Laboulbeniales) from tropical American bat flies (Diptera, Streblidae), revealed by morphology and phylogenetic reconstruction. Mycologia 115: 714.

DOI: 10.1080/00275514.2023.2230114

Danny Haelewaters, André De Kesel (2020)
Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including Hesperomyces halyziae and Laboulbenia quarantenae spp. nov.. MycoKeys 71: 23.

DOI: 10.3897/mycokeys.71.53421

Danny Haelewaters, Thomas J. Matthews, Joseph P. Wayman, Jonathan Cazabonne, Felix Heyman, C. Alisha Quandt, Thomas E. Martin (2024)
Biological knowledge shortfalls impede conservation efforts in poorly studied taxa—A case study of Laboulbeniomycetes. Journal of Biogeography 51: 29.

DOI: 10.1111/jbi.14725

Sergi Santamaria, Jan Pedersen (2021)
Laboulbeniomycetes (Fungi, Ascomycota) of Denmark. European Journal of Taxonomy 781: 1.

DOI: 10.5852/ejt.2021.781.1583

Meredith Blackwell, Danny Haelewaters, Donald H. Pfister (2020)
Laboulbeniomycetes: Evolution, natural history, and Thaxter’s final word. Mycologia 112: 1048.

DOI: 10.1080/00275514.2020.1718442

Miguel A. Naranjo‐Ortiz, Toni Gabaldón (2019)
Fungal evolution: major ecological adaptations and evolutionary transitions. Biological Reviews 94: 1443.

DOI: 10.1111/brv.12510

W. Rossi, B. Guéorguiev, G. Georgiev, D. Stoianova (2019)
Laboulbeniales (Ascomycota) from Bulgaria and other countries. Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology 153: 48.

DOI: 10.1080/11263504.2018.1454531

Jonathan Cazabonne, Lachlan Bartrop, Glen Dierickx, Yusufjon Gafforov, Tina A. Hofmann, Thomas E. Martin, Meike Piepenbring, Mauro Rivas-Ferreiro, Danny Haelewaters (2022)
Molecular-Based Diversity Studies and Field Surveys Are Not Mutually Exclusive: On the Importance of Integrated Methodologies in Mycological Research. Frontiers in Fungal Biology 3: .

DOI: 10.3389/ffunb.2022.860777

Joseph W. Spatafora, M. Catherine Aime, Igor V. Grigoriev, Francis Martin, Jason E. Stajich, Meredith Blackwell, Joseph Heitman, Timothy Y. James (2017)
The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies. Microbiology Spectrum 5: .

DOI: 10.1128/microbiolspec.FUNK-0053-2016

Nalin N. Wijayawardene, Kevin D. Hyde, Kunhiraman C. Rajeshkumar, David L. Hawksworth, Hugo Madrid, Paul M. Kirk, Uwe Braun, Rajshree V. Singh, Pedro W. Crous, Martin Kukwa, Robert Lücking, Cletus P. Kurtzman, Andrey Yurkov, Danny Haelewaters, André Aptroot, H. Thorsten Lumbsch, Einar Timdal, Damien Ertz, Javier Etayo, Alan J. L. Phillips, Johannes Z. Groenewald, Moslem Papizadeh, Laura Selbmann, Monika C. Dayarathne, Gothamie Weerakoon, E. B. Gareth Jones, Satinee Suetrong, Qing Tian, Rafael F. Castañeda-Ruiz, Ali H. Bahkali, Ka-Lai Pang, Kazuaki Tanaka, Dong Qin Dai, Jariya Sakayaroj, Martina Hujslová, Lorenzo Lombard, Belle D. Shenoy, Ave Suija, Sajeewa S. N. Maharachchikumbura, Kasun M. Thambugala, Dhanushka N. Wanasinghe, Bharati O. Sharma, Subhash Gaikwad, Gargee Pandit, Laura Zucconi, Silvano Onofri, Eleonora Egidi, Huzefa A. Raja, Rampai Kodsueb, Marcela E. S. Cáceres, Sergio Pérez-Ortega, Patrícia O. Fiuza, Josiane Santana Monteiro, Larissa N. Vasilyeva, Roger G. Shivas, Maria Prieto, Mats Wedin, Ibai Olariaga, Adebola Azeez Lateef, Yamini Agrawal, Seyed Abolhassan Shahzadeh Fazeli, Mohammad Ali Amoozegar, Guo Zhu Zhao, Walter P. Pfliegler, Gunjan Sharma, Magdalena Oset, Mohamed A. Abdel-Wahab, Susumu Takamatsu, Konstanze Bensch, Nimali Indeewari de Silva, André De Kesel, Anuruddha Karunarathna, Saranyaphat Boonmee, Donald H. Pfister, Yong-Zhong Lu, Zong-Long Luo, Nattawut Boonyuen, Dinushani A. Daranagama, Indunil C. Senanayake, Subashini C. Jayasiri, Milan C. Samarakoon, Xiang-Yu Zeng, Mingkwan Doilom, Luis Quijada, Sillma Rampadarath, Gabriela Heredia, Asha J. Dissanayake, Ruvishika S. Jayawardana, Rekhani H. Perera, Li Zhou Tang, Chayanard Phukhamsakda, Margarita Hernández-Restrepo, Xiaoya Ma, Saowaluck Tibpromma, Luis F. P. Gusmao, Darshani Weerahewa, Samantha C. Karunarathna (2017)
Notes for genera: Ascomycota. Fungal Diversity 86: 1.

DOI: 10.1007/s13225-017-0386-0

Fengming Shi, Sixun Ge, Zehai Hou, Yabei Xu, Jing Tao, Hao Wu, Shixiang Zong (2022)
Species‐specific primers for rapid detection of Monochamus saltuarius, an effective vector of Bursaphelenchus xylophilus in China. Journal of Applied Entomology 146: 636.

DOI: 10.1111/jen.12972

Danny Haelewaters, Walter P. Pfliegler, Michał Gorczak, Donald H. Pfister (2019)
Birth of an order: Comprehensive molecular phylogenetic study excludes Herpomyces (Fungi, Laboulbeniomycetes) from Laboulbeniales. Molecular Phylogenetics and Evolution 133: 286.

DOI: 10.1016/j.ympev.2019.01.007

Timea Nagy, Walter Péter Pfliegler, Attila Takács, Jácint Tökölyi, Attila Molnár V (2019)
Distribution, infection rates and DNA barcoding of Uromyces erythronii (Pucciniaceae), a parasite of Erythronium (Liliaceae) in Europe. Willdenowia 49: 13.

DOI: 10.3372/wi.49.49103

Danny Haelewaters, Alicja Okrasińska, Michał Gorczak, Donald H. Pfister, Antonis Rokas (2020)
Draft Genome Sequence of the Globally Distributed Cockroach-Infecting Fungus Herpomyces periplanetae Strain D. Haelew. 1187d. Microbiology Resource Announcements 9: .

DOI: 10.1128/MRA.01458-19

J. Burazerović, M. Jovanović, Ž. Savković, K. Breka, M. Stupar (2025)
Finding the Right Host in the Darkness of the Cave—New Insights into the Ecology and Spatio-temporal Dynamics of Hyperparasitic Fungi (Arthrorhynchus nycteribiae, Laboulbeniales). Microbial Ecology 88: .

DOI: 10.1007/s00248-025-02521-4

Danny Haelewaters, Peter Boer, Ferenc Báthori, Zoltán Rádai, Ana Sofia P.S. Reboleira, András Tartally, Walter P. Pfliegler, André De Kesel, Oldřich Nedvěd (2019)
Studies of Laboulbeniales onMyrmicaants (IV): host-related diversity and thallus distribution patterns ofRickia wasmannii. Parasite 26: 29.

DOI: 10.1051/parasite/2019028

Jingyu Liu, Danny Haelewaters, Walter P. Pfliegler, Rachel A. Page, Carl W. Dick, M. Catherine Aime (2020)
A new species ofGloeandromycesfrom Ecuador and Panama revealed by morphology and phylogenetic reconstruction, with a discussion of secondary barcodes in Laboulbeniomycetes taxonomy. Mycologia 112: 1192.

DOI: 10.1080/00275514.2020.1781496

Henrik Sundberg, Stefan Ekman, Åsa Kruys, M. Gilbert (2018)
A crush on small fungi: An efficient and quick method for obtainingDNAfrom minute ascomycetes. Methods in Ecology and Evolution 9: 148.

DOI: 10.1111/2041-210X.12850

Warre Van Caenegem, André De Kesel, Danny Haelewaters (2023)
Botryandromyces, a morphology-based genus concept scrutinized by molecular data. Mycological Progress 22: .

DOI: 10.1007/s11557-023-01930-4

Piotr Ceryngier, Jerzy Romanowski, Warre Van Caenegem, Danny Haelewaters (2024)
Parasitism of ladybirds by Hesperomyces in the Canary Islands. Arthropod-Plant Interactions 18: 651.

DOI: 10.1007/s11829-024-10040-1

Sergi Santamaria, Henrik Enghoff, Ana Sofia Reboleira (2020)
The first Laboulbeniales (Ascomycota, Laboulbeniomycetes) from an American millipede, discovered through social media. MycoKeys 67: 45.

DOI: 10.3897/mycokeys.67.51811

Warre Van Caenegem, Danny Haelewaters (2024)
New insights into the DNA extraction and PCR amplification of minute ascomycetes in the genus Laboulbenia (Pezizomycotina, Laboulbeniales). IMA Fungus 15: .

DOI: 10.1186/s43008-024-00146-9

I Guswenrivo, S P Tseng, C C Scotty Yang, T Yoshimura (2018)
Development of Multiplex Nested PCR for Simultaneous Detection of Ectoparasitic Fungi Laboulbeniopsis termitarius and Antennopsis gallica on Reticulitermes speratus (Blattodea: Rhinotermitidae). Journal of Economic Entomology 111: 1330.

DOI: 10.1093/jee/toy091

Jérôme M.W. Gippet, Théotime Colin, Julien Grangier, Fiona Winkler, Marjorie Haond, Adeline Dumet, Simon Tragust, Nathalie Mondy, Bernard Kaufmann (2021)
Land-cover and climate factors contribute to the prevalence of the ectoparasitic fungus Laboulbenia formicarum in its invasive ant host Lasius neglectus. Fungal Ecology 51: 101045.

DOI: 10.1016/j.funeco.2021.101045

Danny Haelewaters, Rachel A. Page, Donald H. Pfister (2018)
Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations. Ecology and Evolution 8: 8396.

DOI: 10.1002/ece3.4359

Danny Haelewaters, André De Kesel, Michał Gorczak, Kevin Bao, Gerrit Gort, Serena Y. Zhao, Donald H. Pfister (2019)
Laboulbeniales (Ascomycota) of the Boston Harbor Islands II (and Other Localities): Species Parasitizing Carabidae, and the Laboulbenia flagellata Species Complex. Northeastern Naturalist 25: 110.

DOI: 10.1656/045.025.s906

Alejandra C. Gutierrez, Eliana Ordoqui, Andreas Leclerque, Claudia López Lastra (2020)
A new species of Herpomyces (Laboulbeniomycetes: Herpomycetales) on Periplaneta fuliginosa (Blattodea: Blattidae) from Argentina. Mycologia 112: 1184.

DOI: 10.1080/00275514.2020.1726134

Michel Perreau, Danny Haelewaters, Paul Tafforeau (2021)
A parasitic coevolution since the Miocene revealed by phase-contrast synchrotron X-ray microtomography and the study of natural history collections. Scientific Reports 11: .

DOI: 10.1038/s41598-020-79481-x

Warre Van Caenegem, Piotr Ceryngier, Jerzy Romanowski, Donald H. Pfister, Danny Haelewaters (2023)
Hesperomyces (Fungi, Ascomycota) associated with Hyperaspis ladybirds (Coleoptera, Coccinellidae): Rethinking host specificity. Frontiers in Fungal Biology 3: .

DOI: 10.3389/ffunb.2022.1040102

Walter P. Pfliegler, Judit Fekete, Ferenc Báthori, András Tartally (2016)
First Central European record of the fungusProlixandromyces triandrusSantam. (Ascomycota: Laboulbeniales), a parasite of veliid bugs (Heteroptera: Veliidae), with notes on its biology and DNA barcoding. Aquatic Insects 37: 215.

DOI: 10.1080/01650424.2016.1194434

Martin Nielsen, Ashot Margaryan, Tejs Lind Nielsen, Henrik Enghoff, Morten E Allentoft (2022)
Complete mitochondrial genomes from museum specimens clarify millipede evolution in the Eastern Arc Mountains. Zoological Journal of the Linnean Society 196: 924.

DOI: 10.1093/zoolinnean/zlac058

Jonathan Cazabonne, Allison K. Walker, Jonathan Lesven, Danny Haelewaters (2024)
Singleton-based species names and fungal rarity: Does the number really matter?. IMA Fungus 15: .

DOI: 10.1186/s43008-023-00137-2

Danny Haelewaters, Serena Y. Zhao, Susana Clusella-Trullas, Ted E. Cottrell, André De Kesel, Lukáš Fiedler, Annette Herz, Helen Hesketh, Cang Hui, Regina G. Kleespies, John E. Losey, Ingrid A. Minnaar, Katie M. Murray, Oldřich Nedvěd, Walter P. Pfliegler, C. Lidwien Raak-van den Berg, Eric W. Riddick, David I. Shapiro-Ilan, Rebecca R. Smyth, Tove Steenberg, Paul S. van Wielink, Sandra Viglášová, Zihua Zhao, Piotr Ceryngier, Helen E. Roy (2017)
Parasites of Harmonia axyridis: current research and perspectives. BioControl 62: 355.

DOI: 10.1007/s10526-016-9766-8

Lauren Goldmann, Alex Weir (2018)
Molecular phylogeny of the Laboulbeniomycetes (Ascomycota). Fungal Biology 122: 87.

DOI: 10.1016/j.funbio.2017.11.004

Danny Haelewaters, Maarten Lubbers, André De Kesel (2022)
The haustorium as a driving force for speciation in thallus-forming Laboulbeniomycetes. IMA Fungus 13: .

DOI: 10.1186/s43008-021-00087-7

Danny Haelewaters, Ingrid A. Minnaar, Susana Clusella-Trullas (2016)
First finding of the parasitic fungusHesperomyces virescens(Laboulbeniales) on native and invasive ladybirds (Coleoptera, Coccinellidae) in South Africa. Parasite 23: 5.

DOI: 10.1051/parasite/2016005

Meredith Blackwell, Fernando E. Vega (2018)
Lives within lives: Hidden fungal biodiversity and the importance of conservation. Fungal Ecology 35: 127.

DOI: 10.1016/j.funeco.2018.05.011

Danny Haelewaters, André De Kesel, Donald H. Pfister (2018)
Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Scientific Reports 8: .

DOI: 10.1038/s41598-018-34319-5

Danny Haelewaters, Michał Gorczak, Patricia Kaishian, André De Kesel, Meredith Blackwell (2021)
Encyclopedia of Mycology. : 263.

DOI: 10.1016/B978-0-12-819990-9.00049-4

Joseph W. Spatafora, M. Catherine Aime, Igor V. Grigoriev, Francis Martin, Jason E. Stajich, Meredith Blackwell (2017)
The Fungal Kingdom. : 1.

DOI: 10.1128/9781555819583.ch1

(2020)
21st Century Guidebook to Fungi. Chapter 17: 435.

DOI: 10.1017/9781108776387.017