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Nucleotide composition bias of rDNA sequences as a source of phylogenetic artifacts in Basidiomycota—a case of a new lineage of a uredinicolous Ramularia-like anamorph with affinities to Ustilaginomycotina

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Abstract

A Ramularia-like hyphomycete was discovered on uredinia of Phakopsora ampelopsidis on leaves of wild Ampelopsis brevipedunculata and cultivated Parthenocissus tricuspidata in several cities in Taiwan. The micromorphology of this fungicolous fungus is similar to that of species of the genus Ramularia which are mostly plant parasites but some species grow on rust fungi. Analyses of SSU and LSU rDNA and RPB2 gene sequence data and of ultrastructural features observed by scanning and transmission electron microscopy revealed that the fungus represents a novel lineage within the Ustilaginomycotina. The name Quasiramularia phakopsoricola is proposed for this new species in a new genus, a new family, and a new order. Sequence data obtained for ITS1, 5.8S, and ITS2 rDNA, however, did not match to any known fungal lineage. Bioinformatics analyses showed that these sequence data are extremely GC poor, but most probably do not represent a pseudogene. Extreme deviations of GC content can be observed in several lineages of Basidiomycota. Such variations affect the results of phylogenetic analyses and are an important source of artifacts.

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Acknowledgements

We thank Y.-H. Yeh, NTU (Taiwan), for technical assistance with DNA methods in the laboratory and M. Basoglu, Goethe University (Germany), for generous help with TEM. We thank P. Kirk (Index Fungorum) for explaining “automatic typification” above the genus rank.

Funding

The study was supported by the Ministry of Science & Technology, Taiwan (NSC 102–2621–B–008–001–MY3 and MOST 109–2621-B-002–004).

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Authors and Affiliations

  1. Institute of Microbiology of the CAS, V.V.I, Vídeňská 1083, Prague, 142 20, Czech Republic

    Miroslav Kolařík

  2. Department of Life Sciences, National Central University, Zhongli, Taoyuan, 320, Taiwan

    I-Chin Wei

  3. Bioresource Collection and Research Center (BCRC), Food Industry Research and Development Institute (FIRDI), Hsinchu, 300, Taiwan

    Sung-Yuan Hsieh

  4. Department of Mycology, Goethe University Frankfurt Am Main, Biologicum, Max-von-Laue-Str. 13, 60438, Frankfurt am Main, Germany

    Meike Piepenbring

  5. School of Forestry and Resource Conservation, National Taiwan University, Taipei, 10617, Taiwan

    Roland Kirschner

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Contributions

Methodology and writing concerning rDNA features such as phylogeny, GC content, and ITS features: Miroslav Kolařík. Formal analysis and investigation particularly of morphology for master thesis: I-Chin Wei. Methodology of electron microscopy: Sung-Yuan Hsieh. Writing—review and editing as well as resources in Germany: Meike Piepenbring. Conceptualization and supervision of study, funding acquisition, collection and deposit of materials, ultrastructure of conidiogenesis, writing the original draft: Roland Kirschner.

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Supplementary Information

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Supplementary file1 Datasets used in the phylogenetic analyses presented in Fig. 1 and ESM 4. (RAR 137 KB)

11557_2021_1749_MOESM2_ESM.xlsx

Supplementary file2 Table S1. GC content of ITS1, 5.8S, ITS2, LSU and SSU of Quasiramularia and other sequences from GenBank belonging to Basidiomycota. (XLSX 30837 KB)

11557_2021_1749_MOESM3_ESM.pptx

Supplementary file3 Figure S1. Secondary structure prediction of ITS2 rDNA sequence from Q. phakopsoricola R. Kirschner 4704. (PPTX 334 KB)

11557_2021_1749_MOESM4_ESM.docx

Supplementary file4 Table of DNA sequences used for the phylogenetic analyses and alternative phylogenetic trees. (DOCX 296 KB)

11557_2021_1749_MOESM5_ESM.rar

Supplementary file5 Datasets of rDNA sequences of Quasiramularia and other sequences from GenBank belonging to Basidiomycota used for the GC content calculation (RAR 5508 KB)

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Kolařík, M., Wei, IC., Hsieh, SY. et al. Nucleotide composition bias of rDNA sequences as a source of phylogenetic artifacts in Basidiomycota—a case of a new lineage of a uredinicolous Ramularia-like anamorph with affinities to Ustilaginomycotina. Mycol Progress 20, 1553–1571 (2021). https://doi.org/10.1007/s11557-021-01749-x

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