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. 2021 Nov 20;62(6):390–394. doi: 10.47371/mycosci.2021.07.001

Phylogeny and taxonomy of Podosphaera filipendulae (Erysiphaceae) revisited

Shu-Yan Liu a, Danni Jin a, Monika Götz b, Michael Bradshaw c, Miao Liu d, Susumu Takamatsu e,*, Uwe Braun f
PMCID: PMC9721504  PMID: 37090177

Abstract

The phylogeny and taxonomy of Podosphaera filipendulae (including P. filipendulensis, syn. nov.) have been examined. Asian, European and North American collections were examined and the nucleotides sequences of their partial rDNA region were determined. In particular, the relationship between P. filipendulae and P. spiraeae was analysed. The results confirmed P. filipendulae and P. spiraeae as two separate, morphologically similar species. The phylogenetic analysis revealed a similar phylogeny to that of the host genera. Although ITS sequences retrieved from Asian, European and North American specimens of P. filipendulae on various Filipendula spp. are identical to sequences from P. macularis on hop, there is consistently one base substitution at the 5'-end of 28S rRNA gene between the species. This result provides evidence that the hop powdery mildew and P. filipendulae are biologically and morphologically clearly distinguished, and should be maintained as two separate species.

Keywords: molecular phylogeny, Podosphaera filipendulensis, Podosphaera macularis, Podosphaera spiraeae, powdery mildew

The genus Filipendula comprises about 15 species of perennial herbs distributed in the temperate zone of the Northern Hemisphere (Schanzer, 1994). In the past, Filipendula was treated as a part of the genus Spiraea until its reintroduction as separate genus by Maximowicz (1879). Spiraea is a larger genus of about 80 to 100 deciduous shrub species distributed in the temperate Northern Hemisphere, with a few species in subtropical regions. The highest diversity of Spiraea occurs in Asia, most notably in China (Drábková, Pospíšková, & Businský, 2017). Numerous species are used as popular ornamental shrubs worldwide. Filipendula and Spiraea pertain to the family Rosaceae, but they are not closely allied. Filipendula is a part of the subfamily Rosoideae, but with an isolated position in phylogenetic multilocus analyses, i.e., it does not belong to any tribe (Potter et al., 2007). Spiraea is the type genus of tribe Spiraeeae, which belongs to the subfamily Amygdaloideae (previously Spiraeoideae, Potter et al., 2007; Drábková et al., 2017). Powdery mildews (Erysiphaceae) are common detrimental pathogens on numerous rosaceous host plants. Salmon (1900) assigned powdery mildew on Filipendula vulgaris (as Spiraea filipendula) to Sphaerotheca humuli, followed by Homma (1937), who included Japanese powdery mildews on Filipendula spp. and Spiraea spp. under Sph. humuli. Sawada (1951) described Sph. spiraeae on Spi. thunbergii from Japan. Based on Chinese type material on F. ulmaria, Zhao (1981) introduced the new species Sph. filipendulae. The two species on Filipendula and Spiraea spp. are barely distinguishable morphologically with regard to their asexual or sexual morphs. Therefore, Braun (1987) merged the two species. Later, Braun and Takamatsu (2000) reallocated Sph. spiraeae to Podosphaera. The first comprehensive phylogenetic analysis of powdery mildews on rosaceous hosts suggested that Podosphaera on Filipendula and on Spiraea, although barely distinguishable morphologically, belong to two different clades (Takamatsu, Niinomi, Harada, & Havrylenko, 2010). Based on these results, Braun and Liu (in Liu, 2010) proposed the combination P. filipendulae. A new powdery mildew species, P. filipendulensis, has recently been described from India on F. vestita (Yadav, Verma, & Singh, 2021). The authors compared results of sequence analyses with sequences from P. ferruginea, P. macularis and P. spiraeae, but unfortunately without inclusion of sequences retrieved from P. filipendulae. To clarify the phylogeny, taxonomy, distribution and host range of P. filipendulae, a new phylogenetic examination, with a large sampling effort including collections and sequences from Asia, Europe and North America, has been performed.

The nucleotide sequences of the 5'-end of the 28S rRNA gene (including domains D1 and D2) and internal transcribed spacer (ITS) regions including the 5.8S rRNA gene were determined in this study. Extractions were accomplished by the Chelex method (Walsh, Metzger, & Higuchi, 1991; Hirata & Takamatsu, 1996). In the United States the primers PM10 (Bradshaw & Tobin, 2020) and ITS4 (White, Bruns, Lee, & Taylor, 1990) were used. One sample from Canada (DAOM 984908) was amplified with P7 (Mori, Sato, & Takamatsu, 2000) and PMITS2 (Cunnington, Takamatsu, Lawrie, & Pascoe, 2003). New sequences from this study were deposited in GenBank (Supplementary Table S1). These sequences were aligned with other sequences of the Erysiphaceae using MUSCLE (Edgar, 2004) implemented in MEGA 7 (Kumar, Stecher, & Tamura, 2016). Alignments were further manually refined using the MEGA 7 program and were deposited in TreeBASE (http://www.treebase.org/) under the accession number S28364. Phylogenetic trees were constructed using maximum parsimony (MP) and maximum likelihood (ML) methods as described in Maeda et al. (2021).

The present phylogenetic analyses (Fig. 1; Supplementary Fig. S1), confirmed that P. filipendulae on Filipendula spp. and P. spiraeae on Aruncus spp. and Spiraea spp. pertain to separate highly supported clades. The analyses confirm that they are separate, morphologically similar species, i.e., the asexual and sexual morphs of two taxa are barely distinguishable. These results are in line with the phylogenetic differentiation of the host genera; Filipendula belongs to the family Rosaceae subfamily Rosoideae, and Aruncus and Spiraea belong to subfamily Amygdaloideae [previously Spiraeoideae] (Potter et al., 2007; Drábková et al., 2017). Sequences of P. spiraeae from Argentina, China, Japan and the USA cluster together and form a well-supported clade distant from sequences obtained from P. filipendulae. A single sequence (AF154325, ex VPRI20247, Korea, asexual morph on Spiraea salicifolia; see Cunnington et al., 2003) was identified as“Sph. spiraeae”. This was undoubtedly misidentified, as the specimen only contained the asexual morph, and it clustered with a Japanese sequence of P. minor. Podosphaera minor pertains to Podosphaera sect. Podosphaera (chasmothecial appendages stiff, setiform, apically dichotomously branched), whereas P. spiraeae belongs to sect. Sphaerotheca (chasmothecial appendages mycelioid, not dichotomously branched). The taxonomic affiliation of powdery mildew on Aruncus spp. was previously not clear. Based solely on morphological similarities, Braun (1987) and Nomura (1997) assigned Sphaerotheca collections on Aruncus to Sph. ferruginea. However, phylogenetic studies of Takamatsu et al. (2010) suggested a close relationship to P. spiraeae, which aligns with the phylogenetic affinity of the genus Aruncus (Arunucs is in the tribe Spiraeeae). The present analyses, including new sequences obtained from Podosphaera collections on Aruncus spp., confirmed the inclusion of this powdery mildew in P. spiraeae. Podosphaera ferruginea on Sanguisorba spp. is distantly allied and clusters close to sequences from P. filipendulae (Fig. 1).

Fig. 1 - Phylogenetic analysis of rDNA ITS region for 64 sequences from the genus Podosphaera. This is the maximum likelihood tree among the 34 equally parsimonious trees with 125 steps, which were found using a heuristic search. Horizontal branch lengths are proportional to the number of substitutions that were inferred to have occurred along a particular branch of the tree. Bootstrap values (≥70%) by the maximum parsimony and maximum likelihood methods are shown on and under the branches, respectively. Sequences determined in this study are highlighted in pink color. Sph.: Sphaerotheca, HT: holotype, ET: epitype, TL: tree length, CI: consistency index, RI: retention index, RC: rescaled consistency index, * epitype of Torula botryoides.

Fig. 1 - Phylogenetic analysis of rDNA ITS region for 64 sequences from the genus Podosphaera. This is the maximum likelihood tree among the 34 equally parsimonious trees with 125 steps, which were found using a heuristic search. Horizontal branch lengths are proportional to the number of substitutions that were inferred to have occurred along a particular branch of the tree. Bootstrap values (≥70%) by the maximum parsimony and maximum likelihood methods are shown on and under the branches, respectively. Sequences determined in this study are highlighted in pink color. Sph.: Sphaerotheca, HT: holotype, ET: epitype, TL: tree length, CI: consistency index, RI: retention index, RC: rescaled consistency index, * epitype of Torula botryoides.

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All sequences obtained from Asian, European and North American specimens on various Filipendula spp. are identical and cluster distantly from P. spiraeae. An ex-type rDNA ITS sequence of the recently described P. filipendulensis (Yadav et al., 2021), from India on F. vestita, is 100% identical with all other P. filipendulae sequences, including all sequences from China, the country from which this species was described. Filipendula vestita, the type host of P. filipendulensis, was cited as a host of P. filipendulae in Braun and Cook (2012), which refers to a record from Pakistan. The asexual morph of P. filipendulensis was not described by Yadav et al. (2021) and is, therefore, not comparable with the anamorph of P. filipendulae. All postulated morphological differences between the latter species and P. filipendulensis listed in Yadav et al. (2021: 138, tab. 1) are overlapping, i.e., the corresponding characteristic of P. filipendulensis fall within the variation of these traits in P. filipendulae. The most characteristic features of P. filipendulae, viz., rather long chasmothecial appendages, straight to curved, mycelioid, but not distinctly geniculate-sinuous, at least to some extent arising from the upper half of the fruiting body, and pigmented, with thickened walls towards the base, are also evident in P. filipendulensis. However, the main issue with the introduction of the later species name lies in that sequences of P. filipendulae were not compared with the ex-holotype sequence of P. filipendulensis. On the basis of 100% identical sequences between P. filipendulensis and P. filipendulae, overlapping morphological traits of the sexual morphs, and previous records of the latter species on F. vestita, it is evident that the two taxa are conspecific.

Collections of P. filipendulae on various Filipendula spp. from Asia, Europe and North America agree morphologically and are characterised by having identical rDNA ITS sequence data, suggesting that a single species is involved with a wider host range and geographical distribution. Podosphaera filipendulae sequences are nearly identical to those obtained from hop (P. macularis) providing evidence of a close affinity of the two species and the involvement of two phylogenetically young species. There are various other examples of closely allied species that are indistinguishable solely based on ITS data, such as the Erysiphe aquilegiae compex (Takamatsu, Ito, Shiroya, Kiss, & Heluta, 2015; Bradshaw et al., 2020) and the E. alphitoides clade (Takamatsu et al., 2015). The common hop powdery mildew, P. macularis, is biologically distinct from P. aphanis and P. filipendulae, as previously established by Salmon (1907), who showed in inoculation experiments, using ascospores and conidia of the hop powdery mildew, that cross infections of Potentilla reptans and F. ulmaria were not possible. Furthermore, the two species are morphologically clearly distinguished (chasmothecial appendages usually in the lower half of the fruiting body, thin-walled, pluriseptate, yellowish to brown, asci (2-)4-8-spored in P. macularis, vs. appendages often arising from the upper half of the fruiting body, moderately thick-walled, above all in the lower half, aseptate to sparingly septate, dark brown when mature, asci 6-8-spored in P. filipendulae; Braun & Cook, 2012). A detailed study of the genetic population diversity of the hop powdery mildew based on North American and European samples has recently been published by Gent et al. (2020). Furthermore, this study revealed one base substitution at the #523 nucleotide from the 5'-end of the 28S rRNA gene between the two species, viz., thymine in P. filipendulae vs cytocine in P. macularis. Owing to this result and the clear biological and morphological differences between the hop powdery mildew and the fungus on Filipendula spp., it is justified to maintain P. macularis and P. filipendulae as two different species.

In conclusion, the new phylogenetic analyses support two different species: P. filipendulae on Filipendula spp., which is widespread in the northern hemisphere, and P. spiraeae on Aruncus and Spiraea spp., an Asian species introduced in Europe, North America and South America:

  • Podosphaera filipendulae (Z.Y. Zhao) T.Z. Liu & U. Braun, in Liu, The Erysiphaceae of Inner Mongolia: 205, Chifeng 2010.

≡ Sphaerotheca filipendulae Z.Y. Zhao, Acta Microbiol. Sin. 21: 439, 1981, nom. cons. (Braun 2013: 1331). Holotype: China, Xinjiang Uygur Autonomous Region, Ili Kazakh Autonomous Prefecture, Habahe County, on Filipendula ulmaria, 28 Aug. 1975, Z.Y. Zhao (HMAS 39000).

= Torula botryoides Corda, in Sturm, Deutschl. Fl., III. Abt. Die Pilze Deutschlands, 8. Heft: 77 + T. 35, Nürnberg 1829. Lectotype (designated here, MycoBank, MBT10001615): Corda (1829: Plate 35), original illustration. Epitype (designated here, MycoBank, MBT10001616): Germany, Sachsen, Landkreis Görlitz, Herrnhut, OT Ruppersdorf, on Filipendula ulmaria 21 May 2011, H. Boyle (GLM-F-96874), ex epitype sequence = MZ242069.

≡ Oidium botryoides (Corda) Ces., in Rabenh., Klotzschii Herb. Viv. Mycol., Cent. XVII, no. 1671, Dresden 1852.

= Podosphaera filipendulensis Sa. Yadav, Sanj. K. Verma & Ragv. Singh, Phytotaxa 491: 137, 2021. Holotype: India, Uttarakhand, Chamoli, Valley of Flowers National Park, on Filipendula vestita, Sep. 2017, S. Yadav (AMH 9934).

Description: Braun and Cook (2012: 140).

Illustrations (selection): Nomura (1997: 37, fig. 37), Shin (2000: 249, fig. 86), Liu (2010: 206, Fig. 100). Braun and Cook (2012: 140, fig. 85).

Host range and distribution: On Filipendula angustiloba (Asia, China), F. auriculata (Asia, Japan), F. intermedia (China, Russia [Far East]), F. camtschatica (Japan, Russia [Far East]), F. multijuga (Japan), F. palmata [including F. nuda = F. palmata var. glabra] (Asia, China, Japan, Russia [Far East]), F. purpurea (Asia, Japan), F. rubra (North America, USA [Indiana, New York, Vermont], Canada [Ontario]), F. ulmaria [including subsp. ulmaria, subsp. denudata and subsp. pentapetala] (Asia, Kazakstan; Europe, Austria, Bulgaria, Czech Republic, Denmark, Estonia, Faroe Islands, Finland, France, Germany, Hungary, Italy, Latvia, Lichtenstein, Lithuania, Netherlands, Norway, Poland, Russia, Serbia, Slovakia, Spain, Sweden, Switzerland, UK, Ukraine; North America, Canada [Ontario], USA [Vermont]), F. vestita (India, Pakistan), F. vulgaris (Caucasus, Armenia; Europe, Denmark, Estonia, Germany, Hungary, Lithuania, Portugal, Romania, Slovakia, Spain, Sweden, Switzerland), Rosaceae [Rosoideae].

Notes: Type material of Torula botryoides is not preserved (see Pilát 1938: 145). Therefore, the original illustration of this species is designated as lectotype, and is supplemented by an epitype with an ex-epitype sequence. The type of the recently described Podosphaera filipendulensis has not been re-examined.

  • Podosphaera spiraeae (Sawada) U. Braun & S. Takam., Schlechtendalia 4: 31, 2000.

≡ Sphaerotheca spiraeae Sawada, Bull. Gov. Forest Exp. Sta. Meguro 50: 104, 1951. Lectotype (designated by Braun 1987): Japan, Iwate Pref., Morioka, on Spiraea thunbergii, 27 Jun. 1897, Takahashi (TNS-F-214412). Syntype: IUM. Epitype (designated here, MycoBank, MBT10001617): Japan, Toyama Pref., Kami-ichi, on Spiraea thunbergii, 11 Jun. 1995, Y. Sato (TNS-F-87186 [ex TSU-MUMH s66]); ex epitype sequence - AB026153.

Description: Braun and Cook (2012: 161).

Illustrations (selection): Nomura (1997: 41, fig. 41, 42), Liu (2010: 216, Fig. 106). Braun and Cook (2012: 162, fig. 120).

Host range and distribution (Amano, 1986; Braun & Cook, 2012; Lee, Kim, Hong, & Lee, 2009; Takamatsu et al., 2010; Talgø et al., 2011; Moparthi, Grove, & Bradshaw, 2018; Chater & Woods, 2019): On Aruncus sylvester [= A. asiaticus, A. dioicus var. kamtschaticus, A. sylvester var. vulgaris] (Asia, China, Japan, Korea, Russia [Far East]), Spiraea betulifolia (Asia, Russia [Far East]; Europe, Norway), Spiraea × bumalda (Europe, Slovakia), Spi. cantoniensis (Asia, Japan; South America, Argentina), Spi. japonica (Asia, China, Japan; Europe, UK [Wales]; North America, USA, Washington), Spi. media (Asia, Kazakhstan, Russia [Far East, Siberia]), Spi. palmata [= Spi. digitata] (Asia, Russia [Far East, Siberia]), Spi. prunifolia (Asia, Japan; ?North America, USA), Spi. sericea (Asia, Russia [Far East]), Spi. salicifolia (Asia, Korea, Russia [Far East, Siberia]), Spi. thunbergii (Asia, Japan).

Notes: Podosphaera spiraeae is an Asian species, introduced in Europe, North and South America on cultivated Spiraea spp. Talgø et al. (2011) reported this species from Norway on Spi. betulifolia with chasmothecia. Other reports, above all those based on anamorphic collections, have to be classified as uncertain, i.e., they are in need of confirmation by sequencing. The record of “Podosphaera cf. clandestina” on Spiraea cantoniensis from Argentina (Delhey, Braun, & Kiehr, 2003), based on an asexual morph, most likely belongs to P. spiraeae, which is a phylogenetically proven host of this species in Argentina (Takamatsu et al., 2010). All collections of P. spiraeae on Aruncus refer to A. sylvester (Asian goat's-beard), which has often been synonymous with A. dioicus as subspecific taxon, but we follow the taxonomy in Flora of China, which considers this taxon a species of its own (http://www.efloras.org/florataxon.aspx?flora_id=2&taxon_id=200010639). There are additional doubtful reports of “Sphaerotheca” on Aruncus and Spiraea, such as Sph. macularis on Aruncus sp. (Germany; Amano, 1986), P. leucotricha, asexual morph on Spi. × bumalda in Argentina, Patagonia (Havrylenko & Takamatsu, 2005), Sph. fuliginea on A. sylvester in California (Gardner, Yarwood, & Raabe, 1970), and various unproven records on Spiraea spp. from Europe (Czech Republic, Denmark, Russia; Amano, 1986; Braun, 1995).

Disclosure

The authors declare no conflicts of interest. All the experiments undertaken in this study comply with the current laws of the countries where they were performed.

Supplementary Material

Supplementary Fig. S1
MYC-62-390-s01.pdf (242.1KB, pdf)
Supplementary table S1
MYC-62-390-s02.pdf (65KB, pdf)

Acknowledgements

This work was financially supported in part by the National Natural Science Foundation of China (31970019).

References

  1. Amano (Hirata), K. (1986) .Host range and geographical distribution of the powdery mildew fungi. Japan Scientific Societies Press. [Google Scholar]
  2. Bradshaw, M., Braun, U., Götz, M., Takamatsu, S., Brand, T., Cabrera, M. G., Dirchwolf, P., Kummer, V., Medina, R., Moparthi, S., & Salcedo-Sarmiento, S. (2020) .Contributions to the phylogeny and taxonomy of the Erysiphaceae (powdery mildews) - part 1. Sydowia, 73, 89–112. http://dx.doi.org/10.12905/0380.sydowia73-2020-0089 [Google Scholar]
  3. Bradshaw, M., & Tobin, P. (2020) .Sequencing herbarium specimens of a common detrimental plant pathogen (powdery mildew). Phytopathology, 110, 1248–1254. http://dx.doi.org/10.1094/PHYTO-04-20-0139-PER [DOI] [PubMed] [Google Scholar]
  4. Braun, U. (1987) .A monograph of the Erysiphales (powdery mildews). Beihefte zur Nova Hedwigia, 89, 1–700. [Google Scholar]
  5. Braun, U. (1995) .The powdery mildews (Erysiphales) of Europe. VEB Gustav Fischer Verlag. [Google Scholar]
  6. Braun, U. (2013) . (2210-2232)Proposals to conserve the teleomorph-typified name Blumeriaagainst the anamorph-typified name Oidiumand twenty-two teleomorph-typified powdery mildew species names against competing anamorph-typified names (Ascomycota: Erysiphaceae). Taxon, 62, 1328–1331. [Google Scholar]
  7. Braun, U., & Cook, R. T. A. (2012) .Taxonomic Manual of the Erysiphales (powdery mildews). CBS Biodiversity Series No. 11. Utrecht: CBS-KNAW Fungal Biodiversity Centre. [Google Scholar]
  8. Braun, U., & Takamatsu, S. (2000) .Phylogeny of Erysiphe, Microsphaera, Uncinula(Erysipheae) and Cystotheca, Podosphaera, Sphaerotheca, (Cystotheceae) inferred from rDNA ITS sequences - some taxonomic consequences. Schlechtendalia, 4, 1–33. [Google Scholar]
  9. Chater, A. O., & Woods, R. G. (2019) .The Powdery Mildews (Erysiphales) of Wales: an identification guide and census catalogue. A. O. Chater, Aberystwyth. [Google Scholar]
  10. Corda, A. C. I. (1829) .Die Pilze Deutschlands. In Sturm, J. [ed.], Deutschlands Flora in Abbildungen nach der Natur mit Beschreibungen, 2, 1–136. Published by Sturm,J., Nürnberg. [Google Scholar]
  11. Cunnington, J. H., Takamatsu, S., Lawrie, A. C., & Pascoe, I. G. (2003) .Molecular identification of anamorphic powdery mildew fungi. Australasian Plant Pathology, 32, 421–428. [Google Scholar]
  12. Delhey, R., Braun, U., Kiehr, M. (2003) .Some new records of powdery mildew fungi from Argentina (2). Schlechtendalia, 10, 79–90. [Google Scholar]
  13. Drábková, L. Z., Pospíšková, M., & Businský, R. (2017) .Phylogeny and infrageneric delimitation in Spiraea (Rosaceae) inferred from AFLP markers and a comparison with morphology. Botanical Journal of the Linnean Society, 185, 525–541. https://doi.org/10.1093/botlinnean/box071 [Google Scholar]
  14. Edgar, R. C. (2004) .MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. http://dx.doi.org/10.1093/nar/gkh340 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gardner, M. W., Yarwood, C. E., & Raabe, R. D. (1970) .Unreported powdery mildews. IV. Plant Disease Reporter, 54, 399–402. [Google Scholar]
  16. Gent, D. H., Claassen, B. J., Gadoury, D. M., Grünwald, N. J., Knaus, B. J., Radišek, S., Weldon, W., Wideman, M. S., & Wolfenbarger, S. N. (2020) .Population diversity and structure of Podosphaera macularis in the Pacific Northwestern United Stated and other populations. Phytopathology, 110, 1105–1116. https://doi.org/10.1094/PHYTO-12-19-0448-R [DOI] [PubMed] [Google Scholar]
  17. Havrylenko, M., & Takamatsu, S. (2005) .Notes on Erysiphales (Ascomycetes) from Patagonia, Argentina. Mycoscience, 46, 32–38. [Google Scholar]
  18. Hirata, T., & Takamatsu, S. (1996) .Nucleotide sequence diversity of rDNA internal transcribed spacers extracted from conidia and cleistothecia of several powdery mildew fungi. Mycoscience, 37, 283–288. [Google Scholar]
  19. Homma, Y. (1937) .Erysiphaceae of Japan. Journal of the Faculty of Agriculture Hokkaido University, 38, 183–461. [Google Scholar]
  20. Kumar, S., Stecher, G., & Tamura, K. (2016) .MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33: 1870–1874. https://doi.org/10.1093/molbev/msw054 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lee, S. Y., Kim, W. G., Hong, S. K., & Lee, Y. K. (2009) .Occurrence of goat's-beard powdery mildew caused by Podosphaera ferruginea in Korea. The Plant Pathology Journal, 25, 299–301. https://doi.org/10.5423/PPJ.2009.25.3.299 [Google Scholar]
  22. Liu, T. Z. (2010) .The Erysiphaceae of Inner Mongolia. Inner Mongolia Science and Technology Press, Chifeng. [Google Scholar]
  23. Maeda, M., Meeboon, J., Heluta, V. P., Liu, S. Y., Tang, S. R., & Takamatsu, S. (2021) .Phylogeny and taxonomy of Phyllactinia species (powdery mildew: Erysiphaceae) occurring on the ash trees (Fraxinus spp.). Mycoscience, 62, 268–280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maximowicz, C. I. (1879) .Adnotationes de Spiraeaceis. Acta Horti Petropolensis, 6, 105–261. [Google Scholar]
  25. Moparthi, S., Grove, G. G., & Bradshaw, M. (2018) .First report of powdery mildew on Spiraea japonica caused by Podosphaera spiraeae in the United States. Plant Disease, 102, 1. https://doi.org/10.1094/PDIS-09-17-1419-PDN [Google Scholar]
  26. Mori, Y., Sato, Y., & Takamatsu, S. (2000) .Evolutionary analysis of the powdery mildew fungi using nucleotide sequences of the nuclear ribosomal DNA. Mycologia, 92, 74–93. https://doi.org/10.2307/3761452 [Google Scholar]
  27. Nomura, Y. (1997) .Taxonomical Study of Erysiphaceae of Japan. Yokendo, Tokyo. [Google Scholar]
  28. Pilát, A. (1938) .Seznam druhů hub, popsaných A. C. J. Cordou s udáním originálních exempl ářů, které jsou uloženy v herbáři Národního Musea v Praze. Sboník Narodního Musea v Praze 1B, 10 [Botanica No. 3], 139–170. [Google Scholar]
  29. Potter, D., Eriksson, T., Evans, R. C., Oh, S., Smedmark, J. E. E., Morgan, D. R., Kerr, M., Robertson, K. R., Arsenault, M., Dickinson, T. A., & Campbell, C. S. (2007) .Phylogeny and classification of Rosaceae. Plant Systematics and Evolution, 266, 5–43. http://dx.doi.org/10.1007/s00606-007-0539-9 [Google Scholar]
  30. Salmon, E. (1900) .A monograph of the Erysiphaceae. Memoirs of the Torrey Botanical Club, 9, 1–292. [Google Scholar]
  31. Salmon, S. (1907) .Notes on the hop powdery mildew (Sphaerotheca humili (DC.) Burr.). Journal of Agricultural Science, 2, 327–332. [Google Scholar]
  32. Sawada, K. (1951) .Researches on fungi in the Tohoku district of Japan (I). Bulletin of the Government Forest Experiment Station Meguro, 50, 97–140. [Google Scholar]
  33. Schanzer, I. A. (1994) .Taxonomic revision of the genus Filipendula (Rosaceae). Journal of Japanese Botany, 69, 290–319. [Google Scholar]
  34. Shin, H. D. (2000) .Erysiphaceae of Korea. Plant Pathogens of Korea, 2, 1–320. [Google Scholar]
  35. Takamatsu, S., Ito, H., Shiroya, Y., Kiss, L., & Heluta, V. (2015) .First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) I. The Microsphaera lineage. Mycologia, 107, 475–489. https://doi.org/10.3852/15-007 [DOI] [PubMed] [Google Scholar]
  36. Takamatsu, S., Niinomi, S., Harada, M., Havrylenko, M. (2010) .Molecular phylogenetic analyses reveal a close coevolutionary relationship between Podosphaera(Erysiphales: Erysiphaceae) and its rosaceous hosts. Persoonia, 24, 38–48. https://doi.org/10.3767/003158510X494596 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Talgø, V., Sundheim, L., Gjærum, H. B., Luz Herrero, M., Suthaparan, A., Toppe, B., & Stensvand, A. (2011) .Powdery mildew on ornamental plants and shrubs in Norway. The European Journal of Plant Science and Technology, 5, 86–92. [Google Scholar]
  38. Walsh, P., Metzger, D., & Higuchi, R. (1991) .Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques, 10, 506–513. [PubMed] [Google Scholar]
  39. White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990) .Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics In: Innis M. A., Gelfand, D. H., Sninsky, J. J., & White T. J. (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). Academic Press. [Google Scholar]
  40. Yadav, S., Verma, S. K., & Singh, R. (2021) .A new species of Podosphaera sect. Sphaerotheca subsect. Sphaerotheca from India - first report of powdery mildew causing wilting and ultimately death of leaves of Filipendula vestita. Phytotaxa, 491, 131–142. https://www.biotaxa.org/Phytotaxa/article/view/phytotaxa.491.2.3 [Google Scholar]
  41. Zhao, Z. Y. (1981) .Taxonomic studies on the genus Sphaerotheca of China. IV. New species and new combination on Rosaceae, Labiatae. Acta Microbiologica Sinica, 21, 438–442. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Fig. S1
MYC-62-390-s01.pdf (242.1KB, pdf)
Supplementary table S1
MYC-62-390-s02.pdf (65KB, pdf)

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