Abstract
A total of 103 tree and shrub samples infected with powdery mildew were collected during 2002–2019 from locations within parks, botanical gardens and urban green areas within the Czech Republic and the powdery mildews were morphologically analyzed and identified. The most frequently represented genera were: Erysiphe (27, including former genera Microsphaera and Uncinula), Podosphaera (11, including former genus Sphaerotheca), Phyllactinia (3), Sawadaea (2) and Arthrocladiella (1). New records for the Czech Republic were: E. (U.) arcuata, E. (M.) deutziae, E. (M.) euonymicola, E. (U.) flexuosa, E. (M.) platani, E. (M.) symphoricarpi, E. (M.) vanbruntiana var. sambuci-racemosae, E. (U.) ulmi, Po. amelanchieris, Po. (Sph.) pruinosa and Po. (Sph.) spiraeae. The results were compared with the spectrum of powdery mildew species in the surrounding countries (Slovakia; Hungary; Poland and Germany (Bavaria)).
1. Introduction
Recently, the recognition of the importance of trees and shrubs in parks and urban green areas within cities has been growing. Urban green areas play a crucial role in helping to keep the air clean and improving community well-being. Shrubs and trees are able to remove both harmful gases and particles from the air, whilst promoting a better quality of health and well-being []. Diseases on these trees and shrubs can reduce their durability, and in the most extreme cases totally destroy them (e.g., Pseudomonas syringae pv. aesculi on horse chestnut).
Powdery mildews are biotrophic, highly specialized pathogens, attacking nearly 10,000 species of vascular plants []. Somewhat confounding is the fact that more than one powdery mildew species can parasitize a single host plant. A deeper understanding of the taxonomy of this group has brought about an ever increasing number of powdery mildew species described, which in 2012 stood at 873, including 794 holomorphs; i.e., those with described asexual and sexual morphs []. The taxonomy of this group, after many revisions, is now greatly different, thus complicating some comparisons with historical data. Until the 1990s, the taxonomy and identification of powdery mildew fungi were based primarily on the characteristics of the teleomorph, such as the shape of the appendages on the chasmothecium (cleistothecium), or on the number of asci in the ascocarps []. However, studies under the scanning electron microscope showed an increased importance of the anamorphic forms in the taxonomy of powdery mildews []. Then, studies based on the molecular data, e.g., [,,,], confirmed that the shape of the appendages has a secondary importance. The genus Erysiphe was found to be polyphyletic, the sections Erysiphe, Galeopsidis and Golovinomyces were elevated to generic rank [,,], and sect. Galeopsidis transferred to a new genus Neoerysiphe. On the other hand, Erysiphe sect. Erysiphe, Microsphaera (including Bulbomicrosphaera and Medusosphaera) and Uncinula (including Bulbouncinula, Furcouncinula and Uncinuliella) with pseudoidium anamorphs (hyphal appressoria lobed, conidia formed singly) were united to form Erysiphe emend containing three morphological sections based on shape of chasmothecial appendages, i.e., E. sects Erysiphe, Microsphaera and Uncinula with respectively mycelioid, dichotomously branched and circicinate appendages []. A molecular phylogenetic study of representatives of the genus Erysiphe showed these sections to be non-phylogenetic []. However, the older names are still useful, since those species with uncinula-type and microsphaera-type appendages mostly parasitize trees or shrubs, and those with myceloid appendages occur mostly on herbaceous plants. This suggests that appendage morphology evolved in close relationship with the host []. Indeed, the evolution from ancestral tree-parasites with branched or circinate appendages to those with myceloid appendages seemed to have occurred convergently at multiple times as an adaptation to herb-parasitism [].
A similar situation exists in the genus Podosphaera, when the previous genera, Sphaerotheca and Podosphaera were only distinguished morphologically by having either simple or branched appendages on their chasmothecia. However, according to molecular analysis, they did not form separate monophyletic clades []. Therefore, they were subsumed into a single genus, Podosphaera, having the morphological, but non-phylogenetic sections and subsections Podosphaera sect. Podosphaera, P. sect. Sphaerotheca and P. sect. Sphaerotheca subsect. Magnicellulatae. The same principle applies here, in that P. sect. Podosphaera (appendages branched) occurs mostly on trees or shrubs, whereas P. sect. Sphaerotheca (appendages myceloid) is found mostly on herbaceous plants.
Information about the spectrum of powdery mildew species in the Czech Republic is fragmentary. Klika [] compiled the first Czech monograph on powdery mildews in 1923. Twenty-five species in seven genera with morphological differences were described. They contained five species of Erysiphe (including Blumeria, Golovinomyces and Neoerysiphe); four each of Microsphaera (now E. sect. Microsphaera; only on tree hosts), Trichocladia (now E. sect. Microsphaera; two of them on tree hosts), Uncinula (now E. sect. Uncinula; only on tree hosts), Sphaerotheca (now Podosphaera sect. Sphaerotheca), three of Podosphaera sect. Podosphaera (only on tree hosts) and one of Phyllactinia (only on tree hosts). In addition, Klika [] cited very sporadic collections of powdery mildews by Opitz, Bubák, Kabát and Petrák in the 19th and early 20th centuries in the area of the Czech Republic. In the last 20 years, some notes on the occurrence of new powdery mildew species on trees and shrubs in the Czech Republic were published, e.g., Erysiphe azaleae on Rhododendron spp. [,], Erysiphe palczewskii on Caragana arborescens Lam. [,], powdery mildew on Homalocladium platycladum (F. Muell.) Meisn. [] and contributions to the knowledge of Erysiphe sp. on Catalpa Scopoli in Europe [].
In Slovakia (for a long time part of former Czechoslovakia), Paulech [] published the Slovak monograph of powdery mildews; later it was primarily Pastirčáková and co-workers who made a greater contribution to the study of powdery mildews, especially on trees, e.g., the first recordings of the occurrence of Erysiphe platani on Platanus L. [], of E. magnifica on lili magnolia [], E. arcuata on Carpinus L. [], E. elevata on Catalpa [] and E. flexuosa on Aesculus L. [].
The aims of our work were to provide an up-to-date check-list of powdery mildews on trees and shrubs in the Czech Republic, to compare this with check-lists of neighbouring countries and to point out which new powdery mildew species during the last decades have been spreading on trees and shrubs within and throughout central and eastern Europe.
2. Materials and Methods
2.1. Field Survey
Between 2002 and 2019, samples of leaf materials infected with powdery mildew were collected from trees and shrubs in parks, botanical gardens and urban green areas in the Czech Republic. Figure 1 shows the locations of the collected samples that are analysed microscopically. All the samples are deposited in the collections of Department of Botany, Faculty of Science, Palacký University in Olomouc.
Figure 1.
Map of the locations in the Czech Republic where the samples of powdery mildew infection on trees and shrubs are collected, and boundaries of neighbouring countries.
The Czech survey was compared with check-lists from the following three neighbouring countries: Slovakia by Paulech [], Poland by Dynowska et al. [], Germany/Bavaria by Bresinsky [] and one close non-adjoining country, Hungary by Nagy and Kiss [], as well as some later recordings in these countries.
2.2. Microscopic Analysis of Morphological Characteristics
Pieces (ca. 20 × 20 mm) of severely infected leaves were used for evaluation by light microscopy (Olympus BX60, Japan). The pathogen was not separated from the host tissue, and the microscopy was done on leaf segments fixed in glacial acetic acid (acetic acid 99%; Lach-Ner, Neratovice, Czech Republic) for 48 h, and stored in glycerol (glycerolum 85%; Tamda, Olomouc, Czech Republic). The conidia and conidiophores, mostly on the upper leaf surfaces, were microscopically examined after staining with cotton blue (Methyl Blue, Sigma-Aldrich, Prague, Czech Republic) []. The presence of fibrosin bodies in the conidia were assessed by mounting fresh conidia in 3% KOH (diluted from potassium hydroxide 90%, Fichema, Czech Republic) []. The sexual morph (chasmothecia) was inspected without any staining. In cases where dried leaf samples were analyzed, a modified method of Shin [] was used, i.e., the heating of herbariumised tissues in fuchsine (Sigma-Aldrich, Prague, Czech Republic) in lactic acid (80% Lach-Ner, Neratovice, Czech Republic). For statistical analyses (means, standard deviations and range), 30 measurements of each characteristic (where possible) were calculated using MS Excel (2010).
2.3. Taxonomic Determination
The names of the host plants were used according to Kubát et al. [] and Biolib (www.biolib.cz) and names of the powdery mildews according to the Taxonomic Manual of the Erysiphales [], Mycobank (www.mycobank.org), and in some cases according to recent taxonomic literature.
3. Results
In total, during 2002–2019, 103 samples of trees and shrubs infected by powdery mildew were collected. A list of the host plants complemented with recently valid names of the powdery mildews according to Braun and Cook [], along with their basic morphological characteristics are listed in Table 1. From our survey, it was clear that the upper sides of the leaves were most frequently colonised. However, the chasmothecia were frequently found on the lower sides of leaves. Powdery mildew anamorphs occurred most frequently in spring and summer, while teleomorphs were found mostly in autumn. On trees and shrubs in the Czech Republic our survey confirmed: one species of the genus Arthrocladiella, 27 species of Erysiphe, three species of Phyllactinia, 11 species of Podosphaera and two species of Sawadaea as detailed in Table 2. For simplicity, Table 3 indicates the additional species in each region compared with the Czech Republic. (Thus, species that were recorded in both another country and the Czech Republic do not appear in this Table). Figure 2 shows the leaves of the trees and shrubs with symptoms of powdery mildew, while Figure 3 shows the variability in the shapes of appendages of the chasmothecia of selected powdery mildew species.
Table 1.
List of representatives of trees and shrubs infected by powdery mildews collected during 2002–2019 in the Czech Republic.
Table 2.
List of powdery mildew species collected on trees and shrubs in the Czech Republic with their host plants.
Table 3.
Additional powdery mildews in neighbouring countries compared with Czech survey (this paper).

Figure 2.
Symptoms of powdery mildew infection on hosts examined in our survey cross-referenced to lists of hosts and powdery mildews in Table 1: A—Acer campestre L. (MM), B—Acer negundo L. (BM), C—Acer platanoides L. (MM), D—Acer tataricum L. (BM), E—Aesculus × carnea Zeyh. (MM), F—Aesculus hippocastanum L. (BM), G—Alnus glutinosa (L.) Gaertn. (MM), H—Amelanchier alnifolia (Nutt.) Nutt. ex M. Roem. (MM), I—Amelanchier ovalis Medik. (BM), J—Berberis vulgaris L. (BM), K—Betula pendula Roth (BM), L—Caragana arborescens Lam. (BM), M—Carpinus betulus L. (BM), N—Catalpa bignonioides Walter (VP), O—Cornus mas L. (BM), P—Cornus sanguinea L. (BM), Q—Corylus avellana L. (AV), R—Crataegus monogyna Jacq. (BM), S—Deutzia scabra Thunb. (BM), T—Euonymus europaeus L. (MM), X—Euonymus fortunei (Turcz.) Hand.-Mazz. (MM), Y—Fagus sylvatica L. (BM), Z—Forsythia × intermedia Zabel (VP), AA—Frangula alnus Mill. (MM), AB—Fraxinus excelsior L. (BM), AC—Ligustrum vulgare L. (BM), AD—Lonicera periclymenum L. (BM), AE—Lonicera tatarica L. (VP), AF—Lycium barbarum L. (EK), AG—Mahonia aquifolium (Pursh) Nutt. (BM), AH—Mahoberberis × neubertii C. K. Schneid. (VP), AI—Malus domestica Borkh. (BM), AJ—Platanus × hispanica Münchh. (MM), AK—Populus tremula L. (BM), AL—Prunus insititia L. (MM), AM—Prunus persica (L.) Batsch (BM), AN—Quercus petraea (Matt.) Liebl. (BM), AO—Quercus robur L. (BM), AP—Ribes uva-crispa L. (BS), AQ—Ribes uva-crispa (BM), AR—Robinia pseudoacacia L. (BM), AS—Rhododendron sp. L. (BM), AT—Rhus typhina L. (BM), AX—Rosa multiflora Thunb. (BM), AY—Rosa pendulina L. (MM), AZ—Salix caprea L. (BM), BA—Salix daphnoides Vill. (BM), BB—Salix purpurea L. (AL), BC—Sambucus nigra L. (MM), BD—Sorbus aucuparia L. (BM), BE—Spiraea japonica L. (MM), BF—Symphoricarpos albus (L.) S.F.Blake (MA), BG—Syringa vulgaris L. (BM), BH—Syringa josikaea J.Jacq. ex Rchb.f. (BM), BI—Ulmus minor Mill. (MM), BJ—Viburnum lantana L. (BM), BK—Viburnum opulus L. (BM), BL—Vitis amurenensis Rupr. (BM), BM—Vitis vinifera L. (BM), BN—Vitis vinifera (VP). Photo: AL—Aleš Lebeda, AV—Abigail Vrbovská, BM—Barbora Mieslerová, BS—Božena Sedláková, EK—Eva Křístková, MA—Marie Ascherová, MM—Markéta Michutová, VP—Veronika Petřeková.
Figure 3.
Variability of chasmothecia of selected species: A—Erysiphe adunca var. adunca (Salix caprea, VP), B—Erysiphe alphitoides (Quercus robur, BM), C—Erysiphe arcuata (Carpinus betulus, VP), D—Erysiphe azaleae (Rhododendron sp., MS), E—Erysiphe berberidis var. berberidis (Berberis vulgaris, MM), F—Erysiphe berberidis (Mahonia aquifolium, VP), G—Erysiphe elevata (Catalpa bignonioides, MM), H—Erysiphe euonymi (Euonymus europaeus, MM), I—Erysiphe flexuosa (Aesculus × carnea, JD), J—Erysiphe grossulariae (Ribes uva-crispa, VP), K—Erysiphe lonicerae var. ehrenbergi (Lonicera tatarica, VP), L—Erysiphe necator (Vitis vinifera, VP), M—Erysiphe ornata var. europaea (Betula pendula, VP), N—Erysiphe palczewskii (Caragana arborescens, VP), O—Erysiphe penicillata (Alnus glutinosa, VP), P—Erysiphe platani (Platanus × hispanica, MM), Q—Erysiphe prunastri (Prunus insititia, MM), R—Erysiphe syringae (Ligustrum vulgare, VP), S—Erysiphe syringae (Syringa josikaea, JD), T—Erysiphe tortillis (Cornus mas, MS), U—Erysiphe vanbruntiana var. sambuci-racemosae (Sambucus racemosa, MS), V—Erysiphe ulmi (Ulmus minor, MM), X—Phyllactinia guttata (Corylus avellana, AV), Y—Phyllactinia guttata (penicillate cells, Corylus avellana, AV), Z—Phyllactinia fraxini (Fraxinus excelsior, JD), AA—Phyllactinia orbicularis (Fagus sylvatica, MS), AB—Podosphaera amelanchieris (Amelanchier ovalis, MM), AC—Podosphaera myrtillina (Vaccinium myrtillus, MZ), AD—Sawadaea bicornis (Acer platanoides, MK), AE—Sawadaea tulasnei (Acer tataricum, JD). Photo: AV—Abigail Vrbovská, BM—Barbora Mieslerová, JD—Jitka Dvořáková, MM—Markéta Michutová, MS—Michaela Sedlářová, VP—Veronika Petřeková.
Although the older descriptions of powdery mildews were very broadly based and involved wide host ranges, most of the species described in Klika [] were re-confirmed in our survey as displayed in Table 2. On the other hand, there were several differences as detailed below.
3.1. Sawadaea and Arthrocladiella
In our survey we distinguished two Sawadaea taxa on Acer as the now well-defined species of S. bicornis and S. tulasnei. These two taxa were described by Klika [] by the older names of Uncinula aceris and its var. tulasnei. In our collections, the sexual state was not always present with S. bicornis, but in these cases it was identified on the basis of symptoms. These species were confirmed in the four nearby countries, apart from Poland that recorded only S. tulasnei []. In Slovakia S. bicornis was more frequent [].
Arthrocladiella on Lycium was recorded by Klika [] as Microsphaera mougeotii. It recently occurs in the Czech Republic and surrounding countries [,,,].
3.2. Phyllactinia Species
Only three Phyllactinia species were found in our survey, namely Ph. guttata, Ph. fraxini and Ph. orbicularis, on respectively, Corylus, Fraxinus and Fagus. The differences with our neighbours, see Table 3, show that Slovakia [] had two additional species, Ph. mali and Ph. roboris, but not Ph. orbicularis. Hungary [] had exactly the same results as Slovakia. Poland [] recorded an additional three species, Ph. berberidis, Ph. mali and Ph. roboris, but not Ph. fraxini or Ph. orbicularis. A very different situation was found in Bavaria [], which had seven additional species namely: Ph. berberidis, Ph. betulae, Ph. carpini, Ph. corni, Ph. mali, Ph. marissalii and Ph. populi.
3.3. Erysiphe Species
This group gave rise to most problems in identification, in particular, those genera involving recent name changes. In our survey 27 species of Erysiphe were recorded on trees. Klika [] described the following genera that are now mostly classed as Erysiphe emend; four Uncinula spp. (one of them Sawadaea on Acer), 4 Microsphaera spp. (one now Arthrocladiella on Lycium) and 2 Trichocladia spp. Compared with Klika [], some additional recordings of powdery mildew species (including invasive ones) were detected. Indeed, it is an interesting fact that during the last few decades several new powdery mildew species were described in Europe, frequently due to their introduction from Asia or America. This is well illustrated with Erysiphe species whose hosts, origins and present locations are listed below. New records for the Czech Republic are in bold:
E. (M.) azaleae on Rhododendron; North American origin, first described in England from the 1990s; see Inman et al. [] and later in Bavaria [], Czech Republic [], Poland [], Slovakia [].
E. (M.) deutziae on Deutzia; Asiatic origin, first described in Europe in 2000 [], and later in Bavaria [], Czech Republic (current article), Poland [].
E. (M.) elevata on Catalpa; North American origin, first described in Europe (Hungary) in 2002 [], and later in Bavaria [], both in Czech Republic and Poland [], Slovakia [].
E. (M.) euonymicola on Euonymus fortunei; Asiatic origin, introduced to the Europe at the beginning of the 20th century; Bavaria [], Czech Republic (current article), Poland [].
E. (M.) palczewskii on Caragana; Asiatic origin, in Europe since the 1990s; see Lebeda et al. [] for the Czech Republic, also in Bavaria [], Hungary [], Poland [] and Slovakia [].
E. (M.) platani on Platanus; North American origin, in Europe from 1960s []; later in Bavaria [], Czech Republic (recent article), Hungary [], Poland [] and Slovakia [].
E. (M.) cf. pseudoacaciae on Robinia pseudoacacia; European (Ukrainian) origin, Bavaria [] (unclear finding), Czech Republic (current article).
E. (M.) syringae-japonicae on Syringa; Asiatic origin, in Europe since the 1990s []; later in Poland [].
E. (M.) symphoricarpi on Symphoricarpos; North American origin, in Hungary since the 1980s; see Kiss et al. [], and later in Czech Republic (current article), Poland [] and Slovakia [].
E. (M.) vanbruntiana var. sambuci-racemosae on Sambucus; Asiatic origin, introduced to Europe; see Braun and Cook [], and later in Bavaria [], Czech Republic (current article), Poland [].
E.(U.)arcuata on Carpinus betulus; European origin, recently in Bavaria [], Czech Republic (current article), Poland [], Slovakia [].
E.(U.) flexuosa on Aesculus; North American species first described in Europe by Ale-Agha et al. []; later in Bavaria [], Czech Republic (current article), Hungary [], Poland [], Slovakia [].
E.(U.)ulmi on Ulmus minor; European origin; Czech Republic (current article), Hungary (as E. clandestina []), Germany (as E. clandestina []), Slovakia (as U. clandestina []).
All of these except E. (M.) syringae-japonicae were confirmed in our study, while Klika [] did not mention any of them. However, most of the Erysiphe spp on trees and shrubs were shared with our neighbouring countries. On the other hand, there were several differences. For instance, E. (M.) friesii was present on Rhamnus in all four neighbours as indicated in Table 3. It is highly probable that this species occurs within the area of our republic, and its non-reporting is only due to a lack of examination of the host. In Slovakia there were three other species not recorded in our survey, namely: E. (M.) magnusii on Lonicera, E. (M.) cotini on Cotinus [] and E. (M.) magnifica on Magnolia []; Hungary had the addition of E. (M.) sparsa on Viburnum [], and Poland added E. (M.) hypophylla on Quercus [].
3.4. Podosphaera Species
We recorded the following 11 species of Podosphaera; all were sect. Podosphaera unless stated as sect. Sphaerotheca (Sph.) and those in bold were new records for the Czech Republic: Podosphaera amelanchieris on Amelanchier (not confirmed in Slovakia, Hungary, Poland), Po. (Sph.) aphanis on Rubus, Po. aucupariae on Sorbus, Po. clandestina on Crataegus, Po. leucotricha on Malus, Po. (Sph.) mors-uvae on Ribes, Po. myrtillina on Vaccinium, Po. (Sph.) pannosa on Rosa, Podosphaera (Sph.) pruinosa on Rhus typhina (not confirmed in Slovakia, Poland, Hungary and Bavaria), Podosphaera (Sph.) spiraeae on Spiraea (not confirmed in Hungary, Slovakia), Po. tridactyla on Prunus. In Bavaria Po. (Sph.) niesslii on Sorbus was the only additional Podosphaera sp. not recorded in our country [].
4. Discussion
This was the first detailed study since Klika’s monograph [], that was focussed on the spectrum of powdery mildew species on a selected group of plants in the Czech Republic. Questions had logically arisen as to whether the spectrum had changed and if so, how it had changed, and what were the reasons for the change.
By comparing our results with Klika’s monograph [], it is clear that most of the powdery mildew species on trees and shrubs in our country have occurred here for a long time. Although Klika [] did not distinguish Sawadaea, Arthrocladiella and other genera, this does not mean that these have not occurred previously in our country. This can be due to the historical changes in the taxonomy of powdery mildews, e.g., Arthrocladiella being recorded by the old name of Microsphaera mougeotii. Braun [] placed it in Erysiphe, which was later divided into the three aforementioned genera: Erysiphe, Golovinomyces and Arthrocladiella. Now Arthrocladiella is a monotypic genus containing a single species (A. mougeotii), with Lycium (Solanaceae) as the sole host genus.
The situation with Sawadaea is similar, being recorded as Uncinula aceris in older literature []. Later, the name Sawadaea was introduced [], and its status was proven by molecular sequence analysis [].
Concerning Phyllactinia, there is also the problem of older publications having a very wide definition of some species, e.g., Ph. guttata (= Ph. corylea) has a wide host range in Klika’s monograph []. At the end of the last century, Ph. guttata was recognized as a species complex, consisting of several biological species []. Then, based on a phylogenetic study by Takamatsu et al. [], Braun and Cook [] confined Ph. guttata to Corylus hosts and accepted separate species on single hosts, e.g., the Phyllactinia spp. alnicola, betulae and carpini that they said were present in all or almost all Europe. Indeed, Ph. betulae and Ph. carpini were found in Bavaria [], but Ph. alnicola was not found in our part of Europe. We all did, however, find the genuine Ph. guttata on Corylus spp. Species of Phyllactinia probably prefer much colder regions. For instance, in Wales, Chater and Woods [] recorded 12 Phyllactinia species. Although Scholler et al. [] had described how P. fraxinicola on Fraxinus was introduced into Europe from Eastern Asia, neither this nor any other recently introduced species of Phyllactinia were recorded in our four country surveys.
As explained above, earlier workers recognised the sections of Podosphaera (sects Podosphaera and Sphaerotheca) as full genera. For instance, on trees and shrubs in the Czech Republic, Klika [] described two Sphaerotheca and three Podosphaera species whilst Slovakia [] had four Sphaerotheca and four Podosphaera species. By comparison with Klika’s survey [], the probably newly occurring species in our republic were: Po. amelanchieris, Po. (Sph.) pruinosa and Po. (Sph.) spiraeae and they were also found in Bavaria by Bresinsky []. The discrepancy with Klika’s list is not surprising, because the hosts (respectively Amelanchier, Rhus and Spiraea) are grown here as ornamentals, and would not have been present in Klika‘s time. All three species are missing in both the Hungarian [], and Polish check-lists []. Later however, Piątek [] confirmed Po. spiraeae in Poland.
The most complicated situation is with the genus Erysiphe. As mentioned above, the previous genera Microsphaera and Uncinula were recently made part of the genus Erysiphe; while another problem is the ever-narrowing definitions of particular species. On trees Klika [] described four Uncinula spp. (one of them is now Sawadaea on Acer), 4 Microsphaera spp. (one is now Arthrocladiella on Lycium) and 2 Trichocladia spp. (now Erysiphe spp.).
A complicated situation arises when more than one powdery mildew species can infect one host plant. This is the case with Salix (with E. adunca and E. capreae), Quercus (with E. alphitoides and E. hypophylla), Acer (with S. bicornis and S. tulasnei), Catalpa (with Erysiphe catalpae, E. elevata and Neoerysiphe galeopsidis), Cornus (with Erysiphe pulchra and E. tortilis) and Syringa (with E. syringae and E. syringae-japonicae). Accurate and experienced interpretations of microscopical, as well as molecular analyses, are needed to fully appreciate the results of the valuable research on these species. For instance, the powdery mildews of Erysiphe genus on legumes represent one of the taxonomically most complicated groups within this genus as highlighted by the revision of Braun et al. [].
5. Conclusions
Despite the problems with the naming of powdery mildews on so wide a range of host species, our study both confirmed previously described species and revealed some new records for our country, i.e., Podosphaera (sect. Po.) amelanchieris on Amelanchier, Po. (sect. Po.) pruinosa on Rhus typhina, Po. (sect. Sph.) spiraeae on Spiraea, E. (U.) arcuata on Carpinus, E. (M.) deutziae on Deutzia, E. (M.) euonymicola on Euonymus fortunei, E. (U.) flexuosa on Aesculus, E. (M.) platani on Platanus, E. (M.) symphoricarpi on Symphoricarpos, E. (M.) vanbruntiana var. sambuci-racemosae on Sambucus racemosa and E. (U.) ulmi on Ulmus minor.
Author Contributions
A.L. conceived and designed the study, participated on collecting of samples and supervised elaboration of results; B.M. participated on designing the study, sampling and elaboration of results; M.M., V.P. contributed to the sampling, performed the laboratory analyses (microscopy); B.M., M.S., R.C. and A.L. interpreted the results; B.M., A.L. and R.C. wrote the manuscript; A.L., R.C., B.M. and M.S. revised the manuscript. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by the Ministry of Education, Youth and Sports, Czech Republic, Project No. MSM 6198959215; National Programme of Conservation and Utilization of Genetic Resources of Plants and Microorganisms; and by the Internal Grant Agency of Palacký University in Olomouc, grants IGA_PrF_2018_001; IGA_PrF_2019_004; IGA_PrF_2020_003.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Kabisch, N.; Strohbach, M.; Haase, D.; Kronenberg, J. Urban green space availability in European cities. Ecol. Indicat. 2016, 70, 586–596. [Google Scholar] [CrossRef]
- Braun, U.; Cook, R.T.A. Taxonomic manual of the Erysiphales (powdery mildews). In CBS Biodiversity Series; CBS-KNAW Fungal Biodiversity Centre: Utrecht, The Netherlands, 2012; Volume 11, pp. 1–707. ISBN 9789070351892. [Google Scholar]
- Braun, U. The Powdery Mildews (Erysiphales) of Europe; Gustav Fischer: Stuttgart, Germany, 1995; ISBN 3334609944. [Google Scholar]
- Cook, R.T.A.; Inman, A.J.; Billings, C. Identification of anamorphs of powdery mildews using morphological and host range data. Mycol. Res. 1997, 101, 975–1002. [Google Scholar] [CrossRef]
- Takamatsu, S.; Hirata, T.; Sato, Y. Phylogenetic analysis and predicted secondary structures of the rDNA internal transcribed spacers of the powdery mildew fungi (Erysiphaceae). Mycoscience 1998, 39, 441–453. [Google Scholar] [CrossRef]
- Saenz, G.S.; Taylor, J.W. Phylogeny of the Erysiphales (powdery mildew) interferred from internal transcribed spacer (ITS) ribosomal DNA sequences. Can. J. Bot. 1999, 77, 150–169. [Google Scholar] [CrossRef]
- Mori, Y.; Sato, Y.; Takamatsu, S. Evolutionary analysis of the powdery mildew fungi (Erysiphales) using nucleotide sequences of the nuclear ribosomal DNA. Mycologia 2000, 92, 74–93. [Google Scholar] [CrossRef]
- Takamatsu, S. Phylogeny and evolution of the powdery mildew fungi (Erysiphales, Ascomycota) inferred from nuclear ribosomal DNA sequences. Mycoscience 2004, 45, 147–157. [Google Scholar] [CrossRef]
- Braun, U. Some critical notes on the classification and generic concept of the Erysiphaceae. Schlechtendalia 1999, 3, 49–55. [Google Scholar]
- Braun, U.; Takamatsu, S. Phylogeny of Erysiphe, Microsphaera, Uncinula (Erysipheae) and Cystotheca, Podosphaera, Sphaerotheca (Cystotheceae) inferred from rDNA ITS sequences; some taxonomic consequences. Schlechtendalia 2000, 4, 1–33. [Google Scholar]
- Braun, U.; Cook, R.T.A.; Inman, A.J.; Shin, H.-D. The taxonomy of the powdery mildew fungi. In The Powdery Mildews. A Comprehensive Treatise; Bélanger, R.R., Bushnell, W.R., Dik, A.J., Carver, T.L.W., Eds.; APS Press: Saint Paul, MN, USA, 2002; pp. 13–55. ISBN 978-0890542910. [Google Scholar]
- Takamatsu, S. Molecular phylogeny reveals phenotypic evolution of powdery mildews (Erysiphales, Ascomycota). J. Gen. Plant Pathol. 2013, 79, 218–226. [Google Scholar] [CrossRef]
- Takamatsu, S.; Hirata, T.; Sato, Y. A parasitic transition from trees to herbs occurred at least twice in tribe Cystotheceae (Erysiphaceae): Evidence from nuclear ribosomal DNA. Mycol. Res. 2000, 104, 1304–1311. [Google Scholar] [CrossRef]
- Klika, J. Monografie Českých Padlí; Masarykova Akademie Práce: Praha, Czech Republic, 1923; Volume 23, pp. 1–80. [Google Scholar]
- Lebeda, A.; Sedlářová, M.; Jankovský, L.; Shin, H.D. First report of rhododendron powdery mildew on Rhododendron spp. in the Czech Republic. Plant Pathol. 2007, 56, 354. [Google Scholar] [CrossRef]
- Sedlářová, M.; Stojaspal, K.; Lebeda, A. Biology of Erysiphe azaleae on Rhododendron luteum in the Czech Republic. Mykol. Listy 2007, 101, 34. [Google Scholar]
- Lebeda, A.; Mieslerová, B.; Sedlářová, M.; Pejchal, M. Occurrence of Anamorphic and Teleomorphic State of Erysiphe palczewskii (syn. Microsphaera palczewskii) on Caragana arborescens in the Czech Republic and Austria and its Morphological Characterization. Plant Prot. Sci. 2008, 44, 41–48. [Google Scholar] [CrossRef]
- Lebeda, A.; Mieslerová, B.; Sedlářová, M. First report of Erysiphe palczewskii on Caragana arborescens in the Czech Republic. Plant Pathol. 2008, 57, 779. [Google Scholar] [CrossRef]
- Lebeda, A.; Mieslerová, B.; Rybka, V.; Sedlářová, M.; Petrželová, I. First record of powdery mildew on Homalocladium platycladum in the Czech Republic. Plant Pathol. 2007, 56, 722. [Google Scholar] [CrossRef]
- Ale-Agha, N.; Bolay, A.; Braun, U.; Feige, B.; Jage, H.; Kummer, V.; Lebeda, A.; Piątek, M.; Shin, H.-D.; Pastirčáková, K. Erysiphe catalpae and Erysiphe elevata in Europe. Mycol. Progr. 2004, 3, 291–296. [Google Scholar] [CrossRef]
- Paulech, C. Flóra Slovenska X/1. Mycota (Huby), Ascomycetes (Vreckaté), Erysiphales (Múčnatkotvaré); Veda, Publishing of Slovak Academy of Sciences: Bratislava, Slovakia, 1995; ISBN 80-224-0412-8. [Google Scholar]
- Pastirčáková, K.; Pastirčák, M.; Adamčíková, K.; Bouznad, Z.; Kedad, A.; El Guilli, M.; Diminic, D.; Hofte, M. Global distribution of Erysiphe platani: New records, teleomorph formation and re-examination of herbarium collections. Cryptogam. Mycol. 2014, 35, 163–176. [Google Scholar] [CrossRef]
- Ondrušková, E.; Juhásová, G.; Pastirčáková, K. The lily magnolia powdery mildew Erysiphe magnifica found in Slovakia. Mycotaxon 2014, 127, 51–57. [Google Scholar] [CrossRef]
- Pastirčáková, K.; Takamatsu, S.; Shiroya, Y.; Pastirčák, M. European hornbeam powdery mildew Erysiphe arcuata in Slovakia. J. Phytopathol. 2008, 156, 597–601. [Google Scholar] [CrossRef]
- Pastirčáková, K.; Pastirčák, M.; Juhásová, G. The Catalpa powdery mildew Erysiphe elevata in Slovakia. Cryptogam. Mycol. 2006, 27, 31–34. [Google Scholar]
- Pastirčáková, K.; Pastirčák, M. Erysiphe flexuosa—A new species of powdery mildew for Slovakia. Biologia 2002, 57, 437–440. [Google Scholar]
- Dynowska, M.; Fiedorowicz, G.; Kubiak, D. Contribution to the distribution of Erysiphales in Poland. Acta Mycol. 1999, 34, 79–88. [Google Scholar] [CrossRef][Green Version]
- Bresinsky, A. Echte Mehltaupilze (Erysiphales) in Bayern–eine vorläufige Übersicht. Ber. Bayer. Bot. Ges. 2016, 86, 163–212. [Google Scholar]
- Nagy, G.S.; Kiss, L. A Check-list of Powdery Mildew Fungi of Hungary. Acta Phytopathol. Entomol. Hungar. 2006, 41, 79–91. [Google Scholar] [CrossRef]
- Lebeda, A.; Reinink, K. Histological characterization of resistance in Lactuca saligna to lettuce downy mildew (Bremia lactucae). Physiol. Mol. Plant Pathol. 1994, 44, 125–139. [Google Scholar] [CrossRef]
- Lebeda, A. The genera and species spectrum of cucumber powdery mildew in Czechoslovakia. J. Phytopathol. 1983, 108, 71–79. [Google Scholar] [CrossRef]
- Shin, H.D. Erysiphaceae of Korea; National Institute Agriculture Science and Technology: Suwon, Korea, 2000; p. 320. [Google Scholar]
- Kubát, K.; Štech, M.; Štěpánek, J. (Eds.) Klíč ke Květeně České Republiky; Academia: Praha, Czech Republic, 2002; ISBN 978-80-200-2660-6. [Google Scholar]
- Piątek, M. Miscellaneous Novelties on Powdery Mildew Fungi from Poland. Pol. Bot. J. 2004, 49, 151–159. [Google Scholar]
- Inman, A.J.; Cook, R.T.A.; Beales, P.A. A contribution to the identity of rhododendron powdery mildew in Europe. J. Phytopathol. 2000, 148, 17–27. [Google Scholar] [CrossRef]
- Shin, H.D.; Mulenko, W. The Record of Erysiphe azaleae (Erysiphales) from Poland and Its Anamorph. Mycobiology 2004, 32, 105–109. [Google Scholar] [CrossRef]
- Bacigálová, K.; Marková, J. Erysiphe azaleae (Erysiphales)—A new species of powdery mildew for Slovakia and further records from the Czech Republic. Czech Mycol. 2006, 58, 189–199. [Google Scholar] [CrossRef]
- Bolay, A.; Braun, U.; Delhay, R.; Kummer, V.; Piatek, M.; Wolczanska, A. Erysiphe deutziae—A new epidemic spread in Europe. Cryptog. Mycol. 2005, 26, 293–298. [Google Scholar]
- Vajna, L.; Fischl, G.; Kiss, L. Erysiphe elevata (syn. Microsphaera elevata), a new North American powdery mildew fungus in Europe infecting Catalpa bignonioides trees. Plant Pathol. 2004, 53, 244. [Google Scholar] [CrossRef]
- Mułenko, W.; Piątek, M.; Wołczańska, A.; Kozłowska, M.; Ruszkiewicz-Michalska, M. Plant parasitic fungi introduced to Poland in modern times. Alien and invasive species. Biol. Invasions Pol. 2010, 1, 49–71. [Google Scholar]
- Vajna, L. First report of powdery mildew on Caragana arborescens in Hungary caused by Erysiphe palczewskii. Plant Pathol. 2006, 55, 814. [Google Scholar] [CrossRef]
- Pastirčáková, K.; Pastirčák, M. Erysiphe platani causing powdery mildew of London plane in Hungary. Acta Phytopathol. Entomol. Hungar. 2008, 43, 31–36. [Google Scholar] [CrossRef]
- Adamska, I. Epidemic of Erysiphe platani in urban areas on the example of the Szczecin (NW Poland). Ecol. Quest. 2019, 30, 71–81. [Google Scholar] [CrossRef]
- Braun, U. Erysiphe miurae and E. syringae-japonicae—New records from Russia. Mikol. Fytopatol. 2002, 36, 15–16. [Google Scholar]
- Piątek, M. Erysiphe azaleae and Erysiphe syringae-japonicae introduced in Poland. Mycotaxon 2003, 87, 121–126. [Google Scholar]
- Kiss, L.; Bolay, A.; Takamatsu, S.; Cook, R.T.A.; Limkaisang, S.; Ale--Agha, N.; Szentiványi, O.; Boal, R.J.; Jeffries, P. Spread of the North American snowberry powdery mildew fungus, Erysiphe symphoricarpi (syn. Microsphaera symphoricarpi), to Europe. Mycol. Res. 2002, 106, 1086–1092. [Google Scholar] [CrossRef]
- Czerniawska, B.; Madej, T. Powdery mildews occurring on barberry, mahonia and snowberry in north--western Poland. Ochrona Roslin 1998, 42, 12. [Google Scholar]
- Sucharzewska, E.; Dynowska, M.; Kubiak, D.; Ejdys, E. Ampelomyces hyperparasites—Occurrence and effect on the development of ascomata of Erysiphales species under conditions of anthropopressure. Acta Soc. Bot. Pol. 2012, 81, 147–152. [Google Scholar] [CrossRef]
- Ale--Agha, N.; Braun, U.; Feige, B.; Jage, H. A new powdery mildew disease on Aesculus spp. introduced in Europe. Cryptog. Mycol. 2000, 21, 89–92. [Google Scholar] [CrossRef]
- Piątek, M. Erysiphe flexuosa, a new for Poland powdery mildew causing disease of Aesculus hippocastanum. Phytopathol. Pol. 2002, 24, 67–71. [Google Scholar]
- Boyle, H.; Klenke, F.; Richter, U. Rediscovery of Erysiphe clandestina on elm (Ulmus) in Germany. Plant Pathol. 2006, 55, 296. [Google Scholar] [CrossRef]
- Homma, Y. Erysiphaceae of Japan. J. Fac. Agric. Hokkaido Univ. 1937, 38, 183–461. [Google Scholar]
- Takamatsu, S.; Inagaki, M.; Niinomi, S.; Khodaparast, S.A.; Shin, H.-D.; Grigaliunaite, B.; Havrylenko, M. Comprehensive molecular phylogenetic analysis and evolution of the genus Phyllactinia (Ascomycota: Erysiphales) and its allied genera. Mycol. Res. 2008, 112, 299–315. [Google Scholar] [CrossRef] [PubMed]
- Chater, O.; Woods, R.G. The Powdery Mildews (Erysiphales) of Wales: An Identification Guide and Census Catalogue; Chater, A.O., Ed.; (Privately Published): Aberystwyth, UK, 2019; ISBN 9780956575036. [Google Scholar]
- Scholler, M.; Schmidt, A.; Meeboon, J.; Braun, U.; Takamatsu, S. Phyllactinia fraxinicola, another Asian fungal pathogen on Fraxinus excelsior (common ash) introduced to Europe? Mycoscience 2018, 59, 85–88. [Google Scholar] [CrossRef]
- Braun, U.; Kruse, J.; Wolcan, S.M.; Murace, M. Three new species of the genus Erysiphe (Ascomycota, Erysiphales) on legumes and some new combinations. Mycotaxon 2010, 112, 173–187. [Google Scholar] [CrossRef]
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