Abstract
Harmoniella junipericola, a new hyphomycete inhabiting on leaf litter of Juniperus chinensis (Cupressaceae) in Japan is described based on morphological characters on natural substrates and in culture and phylogenetic analyses using the sequences of internal transcribed spacer (ITS), large subunit nrRNA gene (LSU; 28S), DNA-directed RNA polymerase I largest subunit gene (RPB1), and DNA-directed RNA polymerase II second largest subunit gene (RPB2). The fungus belongs to the monotypic/monogeneric family Strobiloscyphaceae (one genus with two species; Pezizales) typified by Strobiloscypha. Brief notes are added on morphological and ecological comparisons among H. chrysocephala (type species, in Ukraine), H. campanaensis (in Chile), and H. junipericola. Using the ITS sequences deposited in the DNA Data Bank, additional operational taxonomic units (OTUs) of Harmoniella and phylogenetically related sequences are briefly discussed based on the data from East Asia (Japan, China), Middle East (Israel), Europe (France, Italy, Portugal), and North America (USA).
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Data and material availability
Sequence data are available in the DNA Data Bank (DDBJ/ENA/GenBank; https://www.ddbj.nig.ac.jp/ddbj/index-e.html, https://www.ebi.ac.uk/ena/browser/about, https://www.ncbi.nlm.nih.gov/nuccore) under the accession numbers shown in bold in Table 2. Scientific name of a new species was registered in MycoBank (https://www.mycobank.org/). Specimens and isolates were deposited in herbarium TNS and culture collections JCM and NBRC, respectively, with acronyms explained in the text and Table 2. Alignments used in Figs. 5, 6, and S1 were included in supplementary data.
References
Alshuwaili FE, Al Anbagi RA, Nelsen DJ, Semenova-Nelsen TA, Stephenson SL (2021) Mycobiome sequencing and analysis of the assemblages of fungi associated with leaf litter on the Fernow Experimental Forest in the Central Appalachian Mountains of West Virginia. Curr Res Environ Appl Mycol 11:315–332. https://doi.org/10.5943/cream/11/1/24
Angelini C, Medardi G, Alvarado P (2018) Contribution to the study of neotropical discomycetes: a new species of the genus Geodina (Geodina salmonicolor sp. nov.) from the Dominican Republic. Mycosphere 9:169–177. https://doi.org/10.5943/mycosphere/9/2/1
Borisova VN (1981) Harmoniella, a new genus of hyphomycetes (in Russian). Mikol Fitopat (mycology and Phytopathology) 15:89–92
Carbone M, Agnello C, Alvarado P (2013) Phylogenetic studies in the family Sarcosomataceae (Ascomycota, Pezizales). Ascomycete.org 5:1–12. https://doi.org/10.25664/art-0075
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Chen L, Zhou J, Zeng T, Miao Y-F, Mei L, Yao G-B, Fang K, Dong X-F, Sha T, Yang M-Z, Li T, Zhao Z-W, Zhang H-B (2020) Quantifying the sharing of foliar fungal pathogens by the invasive plant Ageratina adenophora and its neighbours. New Phytol 227:1493–1504. https://doi.org/10.1111/nph.16624
de Hoog GS, Gerrits van den Ende AHG (1998) Molecular diagnostics of clinical strains of filamentous basidiomycetes. Mycoses 41:183–189. https://doi.org/10.1111/j.1439-0507.1998.tb00321.x
Döring H, Clerc P, Grube M, Wedin M (2000) Mycobiont-specific PCR primers for the amplification of nuclear ITS and LSU rDNA from lichenized ascomycetes. Lichenologist 32:200–204. https://doi.org/10.1006/lich.1999.0250
Ekanayaka AH, Hyde KD, Jones EBG, Zhao Q (2018) Taxonomy and phylogeny of operculate discomycetes: Pezizomycetes. Fungal Divers 90:161–243. https://doi.org/10.1007/s13225-018-0402-z
Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327. https://doi.org/10.1016/j.mycres.2005.10.005
GBIF Secretariat (2021) GBIF Backbone Taxonomy. 10.15468/39omei Accessed via https://www.gbif.org/species/5. Accessed 12 Sep 2022
Gomes T, Pereira JA, Lino-Neto T, Bennett AE, Baptista P (2019) Bacterial disease induced changes in fungal communities of olive tree twigs depend on host genotype. Sci Rep 9:5882. https://doi.org/10.1038/s41598-019-42391-8
Hansen K, Perry BA, Dranginis AW, Pfister DH (2013) A phylogeny of the highly diverse cup-fungus family Pyronemataceae (Pezizomycetes, Ascomycota) clarifies relationships and evolution of selected life history traits. Mol Phyl Evol 67:311–335. https://doi.org/10.1016/j.ympev.2013.01.014
Hansen K, Pfister DH (2006) Systematics of the Pezizomycetes—the operculate discomycetes. Mycologia 98:1029–1040. https://doi.org/10.1080/15572536.2006.11832631
Harrington FA, Pfister DH, Potter D, Donoghue MJ (1999) Phylogenetic studies within the Pezizales. I. 18S rRNA sequence data and classification. Mycologia 91:41–50. https://doi.org/10.1080/00275514.1999.12060992
Jeewon R, Yeung QSY, Wannasinghe DN, Rampadarath S, Puchooa D, Wang H-K, Hyde KD (2018) Hidden mycota of pine needles: molecular signatures from PCR-DGGE and ribosomal DNA phylogenetic characterization of novel phylotypes. Sci Rep 8:18053. https://doi.org/10.1038/s41598-018-36573-z
Jeewon R, Yeung QSY, Wannasinghe DN, Rampadarath S, Puchooa D, Wang H-K, Hyde KD (2020) Author correction: Hidden mycota of pine needles: molecular signatures from PCR-DGGE and ribosomal DNA phylogenetic characterization of novel phylotypes. Sci Rep 10:11983. https://doi.org/10.1038/s41598-020-68364-w
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
Kendrick WB, Burges A (1962) Biological aspects of the decay of Pinus sylvestris leaf litter. Nova Hedwigia 4:313–342
Kornerup A, Wanscher JH (1978) Methuen handbook of colour, 3rd edn. Eyre Methuen, London
Kowalski T, Zych P (2002) Endophytic fungi in needles of Pinus nigra growing under different site conditions. Polish Bot J 47:251–257
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol 16:1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
Lumbsch HT, Huhndorf SM (2010) Myconet Volume 14. Part one. Outline of Ascomycota-2009. Part two. Notes on ascomycete systematics. Nos. 4751–5113. Fieldiana Life and Earth Sciences 2010:1–64. https://doi.org/10.3158/1557.1
Madrid H, Torres D, Silva V (2016) Harmoniella campanaensis sp. nov. from central Chile. Mycotaxon 131:535–539. https://doi.org/10.5248/131.535
Matheny PB, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Am J Bot 89:688–698. https://doi.org/10.3732/ajb.89.4.688
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534. https://doi.org/10.1093/molbev/msaa015
Nagao H, Kurogi S, Kiyota E, Sasatomi K (2009) Kumanasamuha geaster sp. nov., an anamorph of Chorioactis geaster from Japan. Mycologia 101:871–877. https://doi.org/10.3852/08-121
Perić B, LoBuglio KF, Pfister DH (2013) The genus Strobiloscypha: a new species and an unresolved phylogenetic placement. Mycol Monten 16:7–22
Perry BA, Hansen K, Pfister DH (2007) A phylogenetic overview of the family Pyronemataceae (Ascomycota, Pezizales). Mycol Res 111:549–571. https://doi.org/10.1016/j.mycres.2007.03.014
Pfister DH, Slater C, Hansen K (2008) Chorioactidaceae: a new family in the Pezizales (Ascomycota) with four genera. Mycol Res 112:513–527. https://doi.org/10.1016/j.mycres.2007.11.016
Pfister DH, Quijada L, LoBuglio KF (2019) Geodina (Pezizomycetes: Wynneaceae) has a single widespread species in tropical America. Fungal Syst Evol 5:131–138. https://doi.org/10.3114/fuse.2020.05.08
Pfister DH, Healy R (2021). Pezizomycetes. In: Zaragoza O (ed) Encyclopedia of Mycology, vol. 1. Elsevier, Oxford, pp 295–309. https://doi.org/10.1016/B978-0-12-819990-9.00054-8
Qadri M, Rajput R, Abdin MZ, Vishwakarma RA, Riyaz-Ul-Hassan S (2014) Diversity, molecular phylogeny, and bioactive potential of fungal endophytes associated with the Himalayan blue pine (Pinus wallichiana). Microb Ecol 67:877–887. https://doi.org/10.1007/s00248-014-0379-4
Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://tree.bio.ed.ac.uk/software/tracer/. Accessed 21 Oct 2022
Rehner SA, Samuels GJ (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycol Res 98:625–634. https://doi.org/10.1016/S0953-7562(09)80409-7
Ronquist F, Teslenko M, van der Mark P, Ayres DL, 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
Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD, Karsch-Mizrachi I (2019) GenBank. Nucleic Acids Res 47:D94–D99. https://doi.org/10.1093/nar/gky989
Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S, Khovanskaya R, Leipe D, Mcveigh R, O’Neill K, Robbertse B, Sharma S, Soussov V, Sullivan JP, Sun L, Turner S, Karsch-Mizrachi I (2020) NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database (Oxford) 2020:baaa062. https://doi.org/10.1093/database/baaa062
Schroers H-J, Samuels GJ, Seifert KA, Gams W (1999) Classification of the mycoparasite Gliocladium roseum in Clonostachys as C. rosea, its relationship to Bionectria ochroleuca, and notes on other Gliocladium-like fungi. Mycologia 91:365–385. https://doi.org/10.1080/00275514.1999.12061028
Schwarz G (1978) Estimating the dimension of a model. Ann Statist 6:461–464. https://doi.org/10.1214/aos/1176344136
Seifert KA, Morgan-Jones G, Gams W, Kendrick B (2011) The genera of hyphomycetes. CBS KNAW Fungal Biodiversity Center, Utrecht
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci USA 94:4520–4525. https://doi.org/10.1073/pnas.94.9.4520
Sugiura N (1978) Further analysis of the data by Akaike’s information criterion and the finite corrections. Commun Stat - Theory Methods 7:13–26. https://doi.org/10.1080/03610927808827599
Sun X, Kosman E, Sharon O, Ezrati S, Sharon A (2020) Significant host- and environment-dependent differentiation among highly sporadic fungal endophyte communities in cereal crops-related wild grasses. Environ Microbiol 22:3357–3374. https://doi.org/10.1111/1462-2920.15107
Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Resour 11:914–921. https://doi.org/10.1111/j.1755-0998.2011.03021.x
Tokumasu S (1978) Leaf litter fungi of the forests of Pinus densiflora and four introduced pines at Sugadaira, central Japan (in Japanese). Trans Mycol Soc Japan 19:383–390
Tokumasu S (1996) Mycofloral succession on Pinus densiflora needles on a moder site. Mycoscience 37:313–321. https://doi.org/10.1007/BF02461303
Tokumasu S, Aoki T, Oberwinkler F (1994) Fungal succession on pine needles in Germany. Mycoscience 35:29–37. https://doi.org/10.1007/BF02268525
Tubaki K (1978) On the Skerman’s micromanipulator and microforge (in Japanese). Trans Mycol Soc Japan 19:237–239
U’Ren JM, Lutzoni F, Miadlikowska J, Arnold AE (2010) Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol 60:340–353. https://doi.org/10.1007/s00248-010-9698-2
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
Weber NS, Denison WC (1995) Western American Pezizales. Strobiloscypha keliae gen. and sp. nov. (Pezizales, Sarcosomataceae) from Oregon. Mycotaxon 54:129–135
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Wijayawardene NN, Hyde KD, Lumbsch HT, Liu JK, Maharachchikumbura SSN, Ekanayaka AH, Tian Q, Phookamsak R (2018) Outline of Ascomycota: 2017. Fungal Divers 88:167–263. https://doi.org/10.1007/s13225-018-0394-8
Wu L, Sun Q, Sugawara H, Yang S, Zhou Y, McCluskey K, Vasilenko A, Suzuki K, Ohkuma M, Lee Y, Robert V, Ingsriswang S, Guissart F, Philippe D, Ma J (2013) Global catalogue of microorganisms (gcm): a comprehensive database and information retrieval, analysis, and visualization system for microbial resources. BMC Genomics 14:933. https://doi.org/10.1186/1471-2164-14-933
Zhu J, Sun X, Tang Q-Y, Zhang Z-D (2021) Seasonal dynamics and persistency of endophyte communities in Kalidium schrenkianum shifts under radiation stress. Front Microbiol 12:778327. https://doi.org/10.3389/fmicb.2021.778327
Acknowledgments
The authors express our great gratitude to Ms. S. Hayashi, Dr. H. Masuya, Mr. T. Mori, Mr. M. Nanjo, Dr. M. Nitta, Ms. S. Ogawa, Ms. N. Sonoda, Ms. A. Suzuki, Mr. K. Taniuchi, and Mr. T. Watanabe for collecting the samples of J. chinensis and Mr. O. Laurence and Dr. K. Nagai for the biological discussion in the early period. The Support Unit for Bio-Material Analysis, RIKEN CBS Research Resources Division is also thanked for technical help with DNA sequencing of JCM strains. The RIKEN Library supported for getting a high-quality copy of a Russian paper. We gratefully acknowledge Prof. K.A. Seifert, two anonymous reviewers, and Prof. R. Kirschner (Section Editor) for their helpful reviews of the manuscript.
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This work was partially supported by the funds obtained from RIKEN Integrated Symbiology (iSYM) and JSPS KAKENHI (Grant Numbers 19H05689 to M.O. and 21K15155 to A.H.).
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Conceived and designed the experiments: T.M., G.O., A.H., Y.D. Field work, morphological and cultural studies: T.M., G.O., Y.D. Molecular work and phylogenetic analyses: A.H. Writing and reviewing the paper: T.M., G.O., A.H., Y.D. Editing the draft: All authors. The final draft was read and approved by all authors.
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List of new taxon names (new species): Harmoniella junipericola Masaki
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Supplementary file1 (PDF 575 kb) Fig. S1 Neighbor-joining tree of Harmoniella spp. based on ITS1 (A) and ITS2 (B) sequences (cf., Tables 2, 3). NJ BS greater than 50% are presented at the nodes. Each taxon is shown in order “strain/sample name”, “collected country”, and “substrate”. The newly obtained sequences are shown in red. The scale bars represent nucleotide substitutions. “*1” indicates the sequences used only for the ITS1 analysis, and “*2” for the ITS2 analysis. “*3” indicates the sequence registered as “Strobiloscypha cupressina” in GenBank
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Masaki, T., Hashimoto, A., Degawa, Y. et al. Harmoniella junipericola (Strobiloscyphaceae, Pezizales), a new hyphomycete inhabiting on leaf litter of Juniperus chinensis in Japan, its molecular phylogenetic classification, and brief notes on other Harmoniella species. Mycol Progress 22, 36 (2023). https://doi.org/10.1007/s11557-023-01884-7
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DOI: https://doi.org/10.1007/s11557-023-01884-7