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Phylogeny and Taxonomy of Podosphaera Filipendulae

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Phylogeny and Taxonomy of Podosphaera Filipendulae Mycoscience VOL.62 (2021) MYC553 Short Communication Phylogeny and taxonomy of Podosphaera filipendulae (Erysiphaceae) revisited Shu-Yan Liua, Danni Jina, Monika Götzb, Michael Bradshawc, Miao Liud, Susumu Takamatsue,*, Uwe Braunf a College of Plant Protection, Jilin Agricultural University, Changchun 130118, Jilin Province, People’s Republic of China b ‌Institute for Plant Protection in Horticulture and Forests, JKI, Julius Kühn-Institute, Federal Research Centre for Cultivated Plants, Messeweg 11/12, 38104 Braun- schweig, Germany c USDA-ARS, Food Quality Laboratory, BARC West, 10300 Baltimore Avenue, Bldg. 002, Beltsville, MD 20705, USA d Biodiversity and Bioresources, Ottawa Research and Development Centre, Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, Canada e Graduate School of Bioresources, Mie University, 1577 Kurima-Machiya, Tsu 514-8507, Japan f Martin Luther University, Institute of Biology, Department of Geobotany and Botanical Garden, Herbarium, Neuwerk 21, 06099 Halle (Saale), Germany 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 sepa- rate, 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 Article history: Received 11 June 2021, Revised 8 July 2021, Accepted 8 July 2021, Available online 6 August 2021 . The genus Filipendula comprises about 15 species of perennial powdery mildew on Filipendula vulgaris (as Spiraea filipendula) to herbs distributed in the temperate zone of the Northern Hemi- Sphaerotheca humuli, followed by Homma (1937), who included sphere (Schanzer, 1994). In the past, Filipendula was treated as a Japanese powdery mildews on Filipendula spp. and Spiraea spp. part of the genus Spiraea until its reintroduction as separate genus under Sph. humuli. Sawada (1951) described Sph. spiraeae on Spi. by Maximowicz (1879). Spiraea is a larger genus of about 80 to 100 thunbergii from Japan. Based on Chinese type material on F. ulmaria, deciduous shrub species distributed in the temperate Northern Zhao (1981) introduced the new species Sph. filipendulae. The two Hemisphere, with a few species in subtropical regions. The highest species on Filipendula and Spiraea spp. are barely distinguishable diversity of Spiraea occurs in Asia, most notably in China morphologically with regard to their asexual or sexual morphs. (Drábková, Pospíšková, & Businský, 2017). Numerous species are Therefore, Braun (1987) merged the two species. Later, Braun and used as popular ornamental shrubs worldwide. Filipendula and Takamatsu (2000) reallocated Sph. spiraeae to Podosphaera. The Spiraea pertain to the family Rosaceae, but they are not closely al- first comprehensive phylogenetic analysis of powdery mildews on lied. Filipendula is a part of the subfamily Rosoideae, but with an rosaceous hosts suggested that Podosphaera on Filipendula and on isolated position in phylogenetic multilocus analyses, i.e., it does Spiraea, although barely distinguishable morphologically, belong not belong to any tribeAdvance (Potter et al., 2007). Spiraea is the type genus Publicationto two different clades (Takamatsu, Niinomi, Harada, & Havrylenko, of tribe Spiraeeae, which belongs to the subfamily Amygdaloideae 2010). Based on these results, Braun and Liu (in Liu, 2010) pro- (previously Spiraeoideae, Porter et al., 2007; Drábková et al., 2017). posed the combination P. filipendulae. A new powdery mildew Powdery mildews (Erysiphaceae) are common detrimental patho- species, P. filipendulensis, has recently been described from India gens on numerous rosaceous host plants. Salmon (1900) assigned 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 * Corresponding author. Graduate School of Bioresources, Mie University, 1577 Kurima-Machiya, Tsu 514-8507, Japan sequences retrieved from P. filipendulae. To clarify the phylogeny, E-mail address: [email protected] (S. Takamatsu). taxonomy, distribution and host range of P. filipendulae, a new This is an open-access paper distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivative 4.0 international license (CC BY-NC-ND 4.0: https://creativecommons.org/licenses/by-nc-nd/4.0/). doi: 10.47371/mycosci.2021.07.001 ― 1 ― S.-Y. Liu et al. / Mycoscience VOL.62 (2021) MYC553 phylogenetic examination, with a large sampling effort including (2021) and is, therefore, not comparable with the anamorph of P. collections and sequences from Asia, Europe and North America, filipendulae. All postulated morphological differences between the has been performed. latter species and P. filipendulensislisted in Yadav et al. (2021: 138, The nucleotide sequences of the 5’-end of the 28S rRNA gene tab. 1) are overlapping, i.e., the corresponding characteristic of P. (including domains D1 and D2) and internal transcribed spacer filipendulensisfall within the variation of these traits in P. filipendu- (ITS) regions including the 5.8S rRNA gene were determined in lae. The most characteristic features of P. filipendulae,viz., rather this study. Extractions were accomplished by the Chelex method long chasmothecial appendages, straight to curved, mycelioid, but (Walsh, Metzger, & Higuchi, 1991; Hirata & Takamatsu, 1996). In not distinctly geniculate-sinuous, at least to some extent arising the United States the primers PM10 (Bradshaw & Tobin, 2020) and from the upper half of the fruiting body, and pigmented, with ITS4 (White, Bruns, Lee, & Taylor, 1990) were used. One sample thickened walls towards the base, are also evident in P. filipendu- from Canada (DAOM 984908) was amplified with P7 (Mori, Sato, & lensis. However, the main issue with the introduction of the later Takamatsu, 2000) and PMITS2 (Cunnington, Takamatsu, Lawrie, species name lies in that sequences of P. filipendulae were not com- & Pascoe, 2003). New sequences from this study were deposited in pared with the ex-holotype sequence of P. filipendulensis.On the GenBank (Supplementary Table S1). These sequences were aligned basis of 100% identical sequences between P. filipendulensisand P. with other sequences of the Erysiphaceae using MUSCLE (Edgar, filipendulae, overlapping morphological traits of the sexual morphs, 2004) implemented in MEGA 7 (Kumar, Stecher, & Tamura, 2016). and previous records of the latter species on F. vestita, it is evident Alignments were further manually refined using the MEGA 7 pro- that the two taxa are conspecific. gram and were deposited in TreeBASE (http://www.treebase.org/) Collections of P. filipendulaeon various Filipendula spp. from under the accession number S28364. Phylogenetic trees were con- Asia, Europe and North America agree morphologically and are structed using maximum parsimony (MP) and maximum likeli- characterised by having identical rDNA ITS sequence data, sug- hood (ML) methods as described in Maeda et al. (2021). gesting that a single species is involved with a wider host range and The present phylogenetic analyses (Fig. 1; Supplementary Fig. geographical distribution. Podosphaera filipendulaesequences are S1), confirmed that P. filipendulaeon Filipendula spp. and P. spiraeae nearly identical to those obtained from hop (P. macularis) provid- on Aruncus spp. and Spiraea spp. pertain to separate highly sup- ing evidence of a close affinity of the two species and the involve- ported clades. The analyses confirm that they are separate, mor- ment of two phylogenetically young species. There are various phologically similar species, i.e., the asexual and sexual morphs of other examples of closely allied species that are indistinguishable two taxa are barely distinguishable. These results are in line with solely based on ITS data, such as the Erysiphe aquilegiae compex the phylogenetic differentiation of the host genera; Filipendula be- (Takamatsu, Ito, Shiroya, Kiss, & Heluta, 2015; Bradshaw et al., longs to the family Rosaceae subfamily Rosoideae, and Aruncus and 2020) and the E. alphitoides clade (Takamatsu et al., 2015). The Spiraea belong to subfamily Amygdaloideae [previously Spiraeoide- common hop powdery mildew, P. macularis, is biologically distinct ae] (Porter et al., 2007; Drábková et al., 2017). Sequences of from P. aphanis and P. filipendulae, as previously established by P. spiraeae from Argentina, China, Japan and the USA cluster to- Salmon (1907), who showed in inoculation experiments, using as- gether and form a well-supported clade distant from sequences cospores and conidia of the hop powdery mildew, that cross infec- obtained
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