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Powdery mildews (Erysiphaceae) on woody plants in urban habitats of Sverdlovsk region (Russia)

Authors:
  • Federal Research Centre the Subtropical Scientific Centre of the Russian Academy of Sciences

Abstract

Based on the results of the authors' research and revisions of previous information, modern species diversity has been established and the first annotated list of powdery fungi on woody plants in urban habitats of Sverdlovsk Region (Ekaterinburg and several cities of the region) has been compiled. Totally, 29 species of Erysiphaceae have been recorded, among which the majority belong to the genus Erysiphe (17 species), and other belong to the genera Podosphaera (7), Phyllactinia (3) and Sawadaea (2). Six species were first found in Sverdlovsk Region: Erysiphe ehrenbergii, E. euonymi, E. lonicerae, E. viburni, Podosphaera myrtillina, and P. spiraeae. Almost half of all identified species (14 of 29) are alien to Sverdlovsk Region, while 6 species can be considered as invasive, of which two species originate from North America (Erysiphe necator and Podosphaera mors-uvae) and four species from East Asia (Erysiphe alphitoides, E. corylacearum, E. palczewskii, and E. vanbruntiana), and another eight species can be considered as unintentionally introduced from neighboring regions together with their host plants. The growth of most species occurs in the period from mid-June to the end of September. The majority of recorded Erysiphaceae species (25 out of 29) form both anamorph and teleomorph, and only four species (Erysiphe aquilegiae, E. necator, Podosphaera pannosa и P. spiraeae) are recorded in the anamorphic stage only.
МИКОЛОГИЯ И ФИТОПАТОЛОГИЯ, 2022, том 56, № 5, с. 323–331
323
POWDERY MILDEWS (ERYSIPHACEAE) ON WOODY PLANTS
IN URBAN HABITATS OF SVERDLOVSK REGION (RUSSIA)
© 2022 T. S. Bulgakova,* and A. G. Shiryaevb,**
aFederal Research Centre the Subtropical Scientific Centre of the Russian Academy of Sciences, 354002 Sochi, Russia
bInstitute of Plant and Animal Ecology of Ural Branch of the Russian Academy of Sciences, 620144 Ekaterinburg, Russia
*e-mail: ascomycologist@yandex.ru
**e-mail: anton.g.shiryaev@gmail.com
Received April 25, 2022; revised May 25, 2022; accepted June 7, 2022
Based on the results of the authors’ research and revisions of previous information, modern species diversity has
been established and the first annotated list of powdery fungi on woody plants in urban habitats of Sverdlovsk
Region (Ekaterinburg and several cities of the region) has been compiled. Totally, 29 species of Erysiphaceae have
been recorded, among which the majority belong to the genus Erysiphe (17 species), and other belong to the gen-
era Podosphaera (7), Phyllactinia (3) and Sawadaea (2). Six species were first found in Sverdlovsk Region: Erysi-
phe ehrenbergii, E. euonymi, E. lonicerae, E. viburni, Podosphaera myrtillina, and P. spiraeae. Almost half of all
identified species (14 of 29) are alien to Sverdlovsk Region, while 6 species can be considered as invasive, of which
two species originate from North America (Erysiphe necator and Podosphaera mo rs-uvae) and four species from
East Asia (Erysiphe alphitoides, E. corylacearum, E. palczewskii, and E. vanbruntiana), and another eight species
can be considered as unintentionally introduced from neighboring regions together with their host plants.
The growth of most species occurs in the period from mid-June to the end of September. The majority of record-
ed Erysiphaceae species (25 out of 29) form both anamorph and teleomorph, and only four species (Erysiphe aq-
uilegiae, E. necator, Podosphaera pannosa и P. spiraeae) are recorded in the anamorphic stage only.
Keywords: alien species, fungal biodiversity, Russia, Urals, urban plantings
DOI: 10.31857/S002636482205004X
INTRODUCTION
Powdery mildews, or erysiphous fungi (division As-
comycota, order Helotiales, family Erysiphaceae) are
common plant pathogens that infect various woody
angiosperms worldwide as obligate plant parasites of
photosynthetic organs of host plants, mainly leaves,
and in some cases – young shoots or twigs, flowers,
and immature fruits (Gorlenko, 1983; Heluta, 1989).
Their presence is usually easy to detect by white patch-
es of mycelium on the surface of affected plant organs
– “powdery mildew” (Gorlenko, 1983; Heluta, 1989;
Braun, Cook, 2012). Although the damage caused by
powdery mildew fungi usually does not lead to the
death of the affected plants, they can often cause a sig-
nificant weakening of host plants, and, consequently,
significant yield losses in fruit and berry crops and es-
pecially reduction in the decorative effect of ornamen-
tal plants (Gorlenko, 1983), including woody plants –
trees and shrubs (Stepanova, Sirko, 1970). The grand
nature transforming in the boreal zone of Eurasia (Le-
skinen, 2020), and relocation of a huge number of cul-
tivated plants in the last two centuries in the Middle
Urals (Tretyakova, 2016) also caused a movement of
many plant pathogenic fungi, including powdery mil-
dews (Desprez-Loustau, 2009). In addition, global cli-
mate warming has led to an increase in the number and
to an expansion of the areas of many cultivated and in-
vasive woody plants over the past decades (Tretyakova,
2016), and at the same time, the further expansion of
new, previously unknown fungal plant pathogens to the
north in the boreal zone of Eurasia (Shiryaev et al.,
2022) and big changes of the mycobiota of Volga-Ural
macroregion (Shiryaev, 2009).
Sverdlovsk Region is located in the south boreal
subzone in the east part of middle Urals on the border
of Europe and Asia and its area is 194.800 km2 (Kapus-
tin, Kornev, 2006). The natural zonal vegetation of the
northern and central parts of the region is represented
by pine and birch forests and mixed broad-leaved-co-
niferous forests, typical for middle and southern taiga
zone; northern forest-steppe vegetation dominates in
the forest-steppe zone in the south part of the region
(Kapustin, Kornev, 2006). The climate of Sverdlovsk
Region is continental, with sharp variability in weather
conditions and clearly defined seasons: warm rainy
summer (the average monthly temperature in July is
19°C) and cold snow winter (the average monthly tem-
perature in January is –13°C). The average annual
temperature is 3.5°С; the average annual rainfall is
600 mm, with a maximum in the summer months
(RIHMI-WDC, 2022).
УДК 582.282.112 : 632.4 (470.54)
БИОРАЗНООБРАЗИЕ,
СИСТЕМАТИКА, ЭКОЛОГИЯ
324
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BULGAKOV, SHIRYAEV
Scientific researches of powdery mildew fungi in
the Urals started at the beginning of the 20th century by
famous Russian mycologist A.A. Yachevsky and his
disciples. Some information those first records of pow-
dery mildew fungi in the territory of the Urals (mainly
modern Perm Region, Komi Republic, Republic of
Bashkortostan, Sverdlovsk Region and Chelyabinsk
Region) is available in “Pocket keybook of fungi. Part
2: Powdery mildew fungi” (Yachevsky, 1927). Howev-
er, there was no one special study of this group of phy-
topathogenic microfungi on the territory of Sverdlovsk
Region and Ekaterinburg City until the 1930s, when
the first information about this group had appeared in
the framework of the first scientific forest pathological
studies (Pentin, 1939). The next step followed in the
1960s, when N.T. Stepanova and A.V. Sirko obtained
and published the most complete checklist of plant-as-
sociated fungi of the Urals that included all available
information on powdery mildew fungi for Sverdlovsk
Region too (Stepanova, Sirko, 1970). However, those
data were very incomplete (especially in comparison
with other regions of the Urals): only seven species of
powdery mildew fungi were recorded on trees and
shrubs in Sverdlovsk Region, and only four species
were found in the Ekaterinburg city (named Sverdlovsk
in 1924–1991). After a long break, E.D. Karelina per-
formed the short study of powdery mildew fungi in
Ekaterinburg in the summer 2016. Despite this re-
search project was short, the total number of Erysipha-
ceae species known in Ekaterinburg on woody plants
has reached 10 species – counting the seven species
first recorded in Ekaterinburg (Karelina, 2017).
However, those data needs to be revised due to the
significantly changes in the taxonomy of powdery mil-
dews during the last two decades. New molecular phy-
logenetic and morphological approaches have helped
to distinguish morphologically similar Erysiphaceae
species and to create an actual system of the family
based on natural relationships of the species (Braun,
1999; Braun, Cooke, 2012; Braun et al., 2019). Thus,
all powdery mildews are treated within the Erysiphace-
ae family (Braun, Takamatsu, 2000), which is placed in
Helotiales now (Johnston et al., 2019). The former sec-
tions of the genus Erysiphe were raised to the genus lev-
el and considered as distinct genera, such as Golovino-
myces and Neoerysiphe (Braun, Takamatsu, 2000;
Takamatsu et al., 2008). Conversely, the genera Micro-
sphaera and Uncinula were both reduced to the mor-
phological sections of the genus Erysiphe (Braun, 1999;
Braun, Cook, 2012), and the same way the genus
Sphaerotheca is treated as morphological section of the
genus Podosphaera now (Braun, Takamatsu, 2000).
Many complex species were resolved, and many new
highly specialized species were described as distinct
fungal species, and many previously described ana-
morphic Erysiphaceae species were replaced in holo-
morphic genera (Braun, Cooke, 2012; Braun et al.,
2018, 2019; Meeboon et al., 2020).
Due to the insufficient completeness of the data on
the diversity of powdery mildews in Sverdlovsk Region,
A.G. Shiryaev and T.S. Bulgakov had continued these
studies since 2020 as part of the study of all plant
pathogenic fungi. Some results of these researches
were published earlier (Bulgakov, Shiryaev, 2021). The
main purpose of the research is to study the modern di-
versity of powdery mildew fungi in Sverdlovsk Region
(including its capital – Ekaterinburg City) parasitizing
on woody plants, and to study their main ecological
and biological features.
MATERIALS AND METHODS
The materials for the study were specimens contain-
ing generative fungal structures (mycelium, conidia
and/or chasmothecia) on affected wild-growing and
cultivated woody plants (leaves, flowers, immature
fruits, and young twigs). The authors also analyzed all
available previous published information on powdery
mildews in Sverdlovsk Region for the last century
(Demidova, 1925; Yachevsky, 1927; Stepanova, Sirko,
1970; Karelina, 2017). All specimens were collected by
A.G. Shiryaev in Ekaterinburg City and some other
towns of Sverdlovsk Region since June to October in
2020 and 2021 in natural (forests) and anthropogenic
locations (public parks, arboreta, block parks, forest
parks, squares and streets), including parks and the ar-
boretum of the Botanical Garden of the Ural Branch of
the Russian Academy of Sciences. The collected spec-
imens – leaves, flowers and fruits affected by powdery
mildews – were labeled, dried at 22–24°C and packed
in paper envelopes according to the standard methods
for the taxon (Heluta, 1989). Totally, 67 fungal speci-
mens of Erysiphaceae on woody plants were collected
and processed in the Institute of Plant and Animal
Ecology of Ural Branch of the Russian Academy of
Sciences (Ekaterinburg) and in the Department of
Plant Protection of the Federal Research Center “Sub-
tropical Scientific Center of the Russian Academy of
Sciences” (Sochi), and later deposed in the fungarium
of the Institute of Plant and Animal Ecology [SVER (F)].
The morphological features of fungal species were
studied according to the standard methods for Erysip-
haceae (Heluta, 1989; Braun, Cook, 2012). All dried
herbarium specimens were examined under optical mi-
croscopes MBI-3 and MICMED-6 (“LOMO”, Rus-
sia) in according to the standard procedures for light
microscopy of temporary preparations (Heluta, 1989;
Braun, Cook, 2012) for the further identification of
fungal species by the morphological examinations of
sexual (chasmothecia) and asexual (conidia) morphs.
The powdery mildew species were identif ied by the
fundamental keybook “Taxonomic manual of the Ery-
siphales” (Braun, Cook, 2012), and some additional
publications devoted to the later performed taxonomi-
cal revisions of the complex species: Erysiphe adunca
(Darsaraei et al., 2021), E. lonicerae (Bradshaw et al.,
2020a), E. viburni (Bradshaw et al., 2020b), and Podo-
МИКОЛОГИЯ И ФИТОПАТОЛОГИЯ том 56 № 5 2022
POWDERY MILDEWS (ERYSIPHACEAE) ON WOODY PLANTS 325
sphaera tridactyla (Meeboon et al., 2020). The host
plant species were identified by the keybook “Keys to
vascular plants of the Middle Urals” (1994) by the
standard methods; the plant species are given accord-
ing to the open nomenclatural database “Plant of the
World” (POWO, 2022).
RESULTS
The annotated checklist of Erysiphaceae on woody
plants in urban planting of Ekaterinburg and other cit-
ies of Sverdlovsk Region is presented (2022). The fun-
gal genera and species are arranged in alphabetical or-
der. The fungal species first found in Sverdlovsk Re-
gion are marked with asterisk; ones new for the region
because of taxonomic revisions of previously recorded
species are marked with hash; ones previously known
on herbaceous plants but first recorded on woody
plants are marked with plus; ones known from previous
publications but not found during authors’ researches
marked with empty round.
The species annotation is given in the following se-
quence: currently accepted fungal species name (the
previously used synonyms are given in parentheses),
host plant name(s), location(s), date(s) of collection,
collection number(s) in the local fungal herbarium
[SVER (F)] or reference(s) for previous record(s); the
note (an.) – if only anamophic stage of the fungal spe-
cies was found; origin for Sverdlovsk Region – for alien
Erysiphaceae species introduced or invaded in Sverd-
lovsk Region (or Europe or Eurasia at general) during
the last century (Desprez-Loustau, 2009; Braun,
Cook, 2012; Farr, Rossman, 2022).
The abbreviations of the locations for the specimens
collected in the Ekaterinburg city: BG – The Botanical
Garden of the Ural Branch of the Russian Academy of
Sciences; BUM – urban microdistrict ‘Botanichesky’;
SFP – forest park ‘Shartashsky’; other locations in
Ekaterinburg city are given without abbreviations.
Erysiphe adunca (Wallr.) Fr. s.str. [= Uncinula salicis
(DC.) G. Winter f. populorum Rabenh.] – Populus species
(Salicaceae): P. × c a n a d e n s i s Moench: 8 March street,
26.09.2021, SVER (F) 96771; P. × s ib i r i ca G.V. Krylov et
G.V. Grig. ex A.K. Skvortsov (Salicaceae): BG, arboretum,
16.10.2020, SVER (F) 96602 (Bulgakov, Shiryaev, 2021);
ibid., 12.08.2021, SVER (F) 96724; Southern tram depot,
02.08.2021, SVER (F) 96723; BUM, 19.10.2021, SVER (F)
96776; Populus balsamifera L., P. deltoides W. Ba rtr am ex
Marshall, P. n ig r a L., and P. tr e m ul a L.: BG, park, Septem-
ber 1960 (Stepanova, Sirko, 1970).
E. alphitoides (Griffon et Maubl.) U. Braun et S. Takam.
( Microsphaera alphitoides Griffon et Maubl.) – Quercus
species (Fagaceae): Q. robur L.: BG, 29.07.2021, SVER (F)
96726 (an.); SFP, 08.08.2016 (Karelina, 2017); Artinsky dis-
trict, forest park near Beryozovskaya, 02.0 9.2021, SVER (F)
96767; Krasnoufimsk district, near Sokolye village, Nizhnei-
rginsk oak forest, 03.09.2021, SVER (F) 96768. Invasive
alien species: invaded Europe and Siberia from Southeast
Asia around 1920 (Takamatsu et al., 2007; Bradshaw et al.,
2022); recorded in Sverdlovsk Region since 1920s (Demido-
va, 1925; Pentin, 1939).
+E. aquilegiae DC. – Clematis species (Ranunculaceae):
Clematis alpina (L.) Mill. subsp. sibirica (L.) Kunt ze ( Atra-
gene sibirica L.): BG, arboretum, 14.08.2021, SVER (F)
96757 (an.); Clematis sp.: BG, arboretum (near greenhouse),
14.10.2020 (Bulgakov, Shiryaev, 2021); recorded on other
herbaceous Clematis species and many herbaceous Ranun-
culaceae (Aconitum, Aquilegia, Delphinium, Ranunculus spe-
cies) in the whole territory of the Urals (Yachevsky, 1927;
Stepanova, Sirko, 1970).
E. berberidis DC. – Berberis species (Berberidaceae):
B. heteropoda Schrenk: BG, meadow, 17.09.2020; DES, pri-
vate garden, 28.09.2020 (Bulgakov, Shiryaev, 2021); B. vul-
garis L.: BG, arboretum, 11.06.2021, SVER (F) 96712; ibid.,
26.10.2020, SVER (F) 96613; BUM, block park, 07.07.2020,
SVER (F) 96612; ibid., 28.06.2021, SVER (F) 96728 (an.);
ibid., 28.07.2021, SVER (F) 96727 (an.); ibid., 29.07.2021,
SVER (F) 96729; Vikulova str., 04.08.2016 (Karelina, 2017).
E. capreae DC. – Salix subgen. Vetri x sect. Vet ri x (Sali-
caceae) (Darsaraei et al., 2020): Salix caprea L.: BG,
19.10.2021, SVER (F) 96775; Artinsky district, forest park
near Beryozovskaya, 02.09.2021, SVER (F) 96766; Salix sp.:
SFP, 08.08.2016 (Karelina, 2017).
E. divaricata (Wallr.) Schltdl. ( Microsphaera divarica-
ta (Wallr.) Lév.) – Frangula alnus Mill. (Rhamnaceae): the
whole territory of the Urals in the habitats of the host plant
(Yachevsky, 1927).
*E. ehrenbergii (Lév.) U. Braun, M. Bradshaw et
S. Takam. ( E. lonicerae DC. var. ehrenbergii (Lév.)
U. Braun et S. Takam.) – Lonicera species subgen. Lonicera
(syn. Chamaecerasus) (Caprifoliaceae): L. caucasica Pall.:
BUM, block park, 22.07.2020 (Bulgakov, Shiryaev, 2021).
Introduced alien species: native for Eurasia (Bradshaw et al.,
2021a), but was introduced in Sverdlovsk Region with the
host plants.
*E. euonymi DC. – Euonymus species (Celastraceae):
E. europaeus L.: BG, arboretum, 14.08.2021, SVER (F)
96758 (an.); ibid., 22.08.2021, SVER (F) 96759. Introduced
alien species: native for Eurasia (Braun, Cook, 2012), but
was introduced in Sverdlovsk Region with the host plant.
*E. lonicerae DC. s. str. [ Microsphaera lonicerae (DC.)
G. Winter] – Lonicera species subgen. Caprifolium (Caprifo-
liaceae): L. caprifolium L.: BG, arboretum, 20.20.2021,
SVER (F) 96777 (an.); Lonicera reticulata Raf.: BG, arbore-
tum, 11.06.2021, SVER (F) 96713 (an.); ibid., 11.06.2021,
SVER (F) 96714 (an.); Lonicera sp.: BUM, 24.07.2021,
SVER (F) 96732 (an.). Introduced alien species: native for
Eurasia (Bradshaw et al., 2021a), but was introduced in
Sverdlovsk Region with the host plants.
E. necator Schwein. [ Uncinula necator (Schwein.) Bur-
rill] – Vitis species (Vitaceae): V. am u r en s is Rupr.: urban mi-
crodistrict ‘Seven fountains’, garden, 21.08.2021, SVER (F)
96760 (an.); V. vinifera L.: BG, arboretum, 10.09.2017 (Bul-
gakov, Shiryaev, 2021); Invasive alien species: invaded in
Europe from North America in the middle of XIX century;
known in the Urals since 1900s (Demidova, 1925;
Yachevsky, 1927).
E. ornata (U. Braun) U. Braun et S. Takam. var. euro-
paea (U. Braun) U. Braun et S. Takam. (= Microsphaera bet-
ulae Magnus) – Betula species (Betulaceae): B. pubescens
Ehrh.: Achit district, forest park near Achitsky, 12.09.1960
(Stepanova, Sirko, 1970); Betula sp.: Vikulova str.,
04.08.2016 (Karelina, 2017).
E. palczewskii (Jacz.) U. Braun et S. Takam. – Caragana
species (Fabaceae): C. arborescens Lam. BUM, block park,
01.07.2021, SVER (F) 96734; ibid., 11.07.2021, SVER (F)
326
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BULGAKOV, SHIRYAEV
96735; Academichesky av., street shrubs, 27.07.2021, SVER
(F) 96736; near the Circus, street shrubs, 07.08.2021, SVER
(F) 96733; Tatishcheva str., block park, 30.07.2016 (Kareli-
na, 2017); Invasive alien species: invaded in European Russia
and Siberia from East Asia about 1980 (Heluta, Gorlenko,
1984).
E. salicis DC. – Salix species (excluding subgen. Vetrix
sect. Vetrix) (Salicaceae): S. viminalis L.: BG, arboretum,
03.08.2020 (Bulgakov, Shiryaev, 2021).
E. syringae-japonicae (U. Braun) U. Braun et S. Takam.
( Microsphaera syringae-japonicae U. Braun) – on Syringa
species (Oleaceae): S. josikaea J. Jacq. ex Rchb.: BG, arbo-
retum, 27.07.2021, SVER(F) 96779; S. villosa Vahl: BUM,
street shrubs, 29.07.2021, SVER (F) 96737 (an.); S. vulgaris
L.: Nagornaya str., street shrubs, 04.08.2016 (Karelina,
2017). Invasive alien species: invaded in Europe and western
Asia in 1980s from Japan (Seko et al., 2008; Takamatsu et al.,
2016); first recorded in Sverdlovsk Region after 2000 (Kare-
lina, 2017).
+E. trifoliorum (Wallr.) U. Braun (= E. trifolii Grev.) – on
Fabaceae species: Chamaecytisus ruthenicus (Fisch. ex Wol.)
Klásk.: Krasnoufimsk district, Sokolye village, Nizheirginsk
oak forest, 03.09.2021, SVER (F) 96769 (an.). This species is
known on herbaceous Fabaceae plants in Sverdlovsk Region
(Yachevsky, 1927; Stepanova, Sirko, 1970; Karelina, 2017),
but first recorded on Chamaecytisus ruthenicus in the Urals.
E. vanbruntiana (W.R. Gerard) U. Braun et S. Takam.
var. sambuci-racemosae (U. Braun) U. Braun et S. Takam. –
Sambucus species: S. racemosa L.: BG, park, 18.06.2021,
SVER (F) 96715; ibid., 12.08.2021, SVER (F) 96738 (an.);
ibid., 23.07.2021, SVER (F) 96739; SFP, 08.08.2016 (Kare-
lina, 2017); S. sibirica Nakai: BG, park, 22.09.2021, SVER
(F) 96770; Invasive alien species: invaded Europe and Sibe-
ria from East Asia about 1980 (Heluta, Gorlenko, 1981).
*E. viburni Duby – Viburnum species (Viburnaceae):
V. l a n t a n a L.: GES, private garden, 30.09.2020 (Bulgakov,
Shiryaev, 2021). Introduced alien species: native for Eurasia
(Braun, Cook, 2012), but was introduced in Sverdlovsk Re-
gion with its host plant.
#?Phyllactinia alnicola U. Braun (= Ph. suffulta Sacc. f.
alni Hammarl.) – on Alnus species (Betulaceae): A. incana
(L.) Moench. and A. glutinosa (L.) Gaertn.: the whole terri-
tory of the Urals (Yachevsky, 1927); Krasnoufimsky district,
near Ufa river, September 1960 (Stepanova, Sirko, 1970).
#Ph. betulae (DC.) Fuss (= Ph. suffulta Sacc. f. betulae
Thüm.) – Betula species (Betulaceae): B. pendula Roth. and
B. pubescens Ehrh.: the whole territory of the Urals
(Yachevsky, 1927); Krasnoufimsky district, Nizhneigrisk
oak forest, August 1960 (Stepanova, Sirko, 1970).
Ph. guttata (Wallr.) Lév. (= Ph. suffulta Sacc f. corylli-
avellanae Jacz.) – Corylus avellana L. (Betulaceae): the
whole territory of the Urals (Yachevsky, 1927).
+Podosphaera aphanis (Wallr.) U. Braun et S. Takam. –
Dasiphora species (Rosaceae): D. fruticosa (L.) Rydb.: BG,
arboretum, 29.07.2021, SVER (F) 96740 (an.); BG,
03.08.2021, SVER (F) 96741 (an.); 8 March str., Arboretum,
29.08.2021, SVER (F) 96763 (an.); D. glabrata (Willd. ex
Schltdl.) Soják: near buildings of ‘Russian Copper Plant’,
flowerbed, 29.08.2021, SVER (F) 96762. This fungal species
was recorded in the Urals (as several forms of Sphaerotheca
macularis (Wallr.) Magnus) on many herbal Rosaceae plants
Alchemilla, Agrimonia, Geum, and Potentilla species
(Yachevsky, 1927; Stepanova, Sirko, 1970; Karelina, 2017).
P. c l a n de s t i na (Wallr.) Lév. (= P. o x ya c a n t h ae De Ваrу f.
crataegi Jacz.) – Crataegus species (Rosaceae): C. mollis
(Torr. et A. Gray) Scheele: BG, arboretum, 05.07.2021,
SVER (F) 96742 (an.); C. sanguinea Pall.: BG, arboretum,
06.07.2021, SVER (F) 96743; BUM, block park, 15.06.2021,
SVER (F) 96716 (an.); ibid., 15.07.2021, SVER (F) 96746.;
Crataegus sp.: Nagornaya str., block park (Karelina, 2017).
P. mors-uvae (Schwein.) U. Braun et S. Takam.
[Sphaerotheca mors-uvae (Schwein.) Berk. et M.A. Curtis]
Ribes species (Grossulariaceae): R. uva-crispa L. (= Gros-
sularia reclinata (L.) Mill.): BG, arboretum, 15.06.1956
(Stepanova, Sirko, 1970); BG, arboretum, 14.09.2020 (Bul-
gakov, Shiryaev, 2021); urban microdistrict “Seven fon-
taines”, 06.06.2021, SVER (F) 96717 (an.); Ribes nigrum L.,
urban microdistrict “Seven fontaines”, 01.07.2021, SVER
(F) 96744 (an.); Ribes rubrum L., the Arboretum on 8 March
str., 04.07.2021, SVER (F) 96745 (an.). Invasive alien spe-
cies: invaded Europe from North America in 1900s (Heluta,
1989; Braun, Cook, 2012); presents in the Ural macroregion
since 1913 (Yachevsky, 1927) and in Sverdlovsk Region at
least since 1956 (Stepanova, Sirko, 1970).
* P. myrtillina KunzeVaccinium myrtillus L. (Ericaceae):
Pervouralsk city district, forest park near Glukhoye lake,
08.08.2021, SVER(F) 96756.
P. pannosa (Wallr.) de Bary Rosa species (Rosaceae):
R. acicularis Lindl.: BUM, 24.07.2021, SVER (F) 96747 (an.);
R. canina L.: BG, park, 24.09.2021, SVER (F) 96772 (an.);
R. chinensis Jacq.: BUM, 29.07.2021, SVER (F) 96748
(an.); Rosa sp.: BG, arboretum, 12.08.2021, SVER (F)
96761 (an.); Kraul str., block park, 04.08.2016 (an.) (Kareli-
na, 2017).
*P. spiraeae (Sawada) U. Braun et S. Takam. – Spiraea
species (Rosaceae): S. chamaedryfolia L.: BG, arboretum,
20.10.2020 (Bulgakov, Shiryaev, 2021); GES, private garden,
21.09.2020; ibid., 28.09.2020 (Bulgakov, Shiryaev, 2021);
BUM, block park, 23.09.2020 (Bulgakov, Shiryaev, 2021);
S. media Schmidt, BUM, 29.07.2021, SVER (F) 96749 (an.);
Spiraea sp., BUM, 06.08.2021, SVER (F) 96750 (an.). Status
and origin of this species is unclear (Braun, Cook, 2012);
previous publications did not mention this species for Sverd-
lovsk Region, however, it is known in East Europe (Braun,
Cook, 2012) and in West Siberia (Tomoshevich, 2015).
P. tridactyla (Wallr.) de Bary s. str. [= Р. t r i d a ct y l a
(Wallr.) De Вагу f. padi Jacz.] – Prunus padus L. (Rosaceae):
BG, park, 18.06.2021, SVER (F) 96718 (an.); ibid.,
05.07.2021, SVER (F) 96752; ibid., 28.07.2021, SVER (F)
96751.
*Sawadaea bicornis (Wallr.) Homma (=Uncinula aceris
DC.) – Acer species (Sapindaceae): A. negundo L.: BUM,
block park, 22.07.2020; BG, arboretum, 14.10.2020 (Bulga-
kov, Shiryaev, 2021); BG, arboretum, 06.06.2021, SVER (F)
96721 (an.); ibid., 11.06.2021, SVER (F) 96719 (an.); ibid,
23.07.2021, SVER (F) 96753 (an.); ibid., 23.07.2021, SVER
(F) 96755 (an.); ibid, 12.08.2021, SVER (F) 96764; BUM,
23.07.2021, SVER (F) 96754 (an.); ibid., 14.06.2021, SVER
(F) 96720 (an.); 8 March str., near the theatre
“Shchelkunchik”, street trees, 21.06.2021, SVER (F) 96722
(an.); A. platanoides L.: BG, arboretum, 22.08.2021, SVER
(F) 96765 (an.). Introduced alien species: native for Eurasia,
but came in Sverdlovsk Region from the Southern Urals to-
gether with its host plants (Acer campestre and A. negundo).
S. tulasnei (Fuckel) Homma – Acer species (Sapinda-
ceae): A. platanoides L.: BUM, block park, 25.10.2020 (Bul-
gakov, Shiryaev, 2021); A. tataricum L.: SFP, 08.08.2016
(an.) (Karelina, 2017). Introduced alien species: native for
Eurasia, but was introduced in Sverdlovsk Region from the
Southern Urals together with its host plants (Acer platanoides
and A. tataricum). S. tulasnei was previously recorded on Ac-
МИКОЛОГИЯ И ФИТОПАТОЛОГИЯ том 56 № 5 2022
POWDERY MILDEWS (ERYSIPHACEAE) ON WOODY PLANTS 327
er negundo in Ekaterinburg (Karelina, 2017); however, these
records are doubtful and require verification because this
species does not usually affect this plant species (Heluta,
1989 ).
DISCUSSION
The number of powdery mildew fungi recorded on
woody plants in Sverdlovsk Region reached 29 species
of four genera in 2022, according to the modern taxo-
nomy of the family Erysiphaceae (Braun, Cook, 2012).
Totally, five species are new for the region as first found
after our researches (Bulgakov, Shiryaev, 2021), and
four species – Erysiphe ehrenbergii, E. salicis, Phyllac-
tinia alnicola, and Ph. betulae – can be considered as
new ones because of taxonomic revisions of previously
known species; three species – Erysiphe aquilegiae,
E. trifoliorum, and Podosphaera aphanis – are first re-
corded on woody host plants in the region, but previ-
ously they were known here on herbaceous plants only
(Yachevsky, 1927; Stepanova, Sirko, 1970; Karelina,
2017). We have also included in the list five species still
known only from old collections and references: Erysi-
phe divaricata, E. ornata, Phyllactinia alnicola, Ph. betu-
lae, and Ph. guttata; almost all of them were collected
in southwestern districts of Sverdlovsk Region in
1920–1960s (Stepanova, Sirko, 1970).
The most numerous genus is Erysiphe (17 species,
58.6%), and other three genera are represented by a
lesser number of species (41.4% only): Podosphaera
(7 species), Phyllactinia (3) and Sawadaea (2). Such di-
versity and taxonomic structure are typical for woody
plants in other boreal regions in the zone of mixed for-
ests of the European Russia with well-studied diversity
of Erysiphaceae: Moscow City and Moscow Region
(Gorlenko, 1983; Blagoveshchenskaya, 2015), Saint-
Petersburg City and Leningrad Region (Cherapanova,
Cherepanov, 2004; Popov et al., 2007; Bulgakov et al.,
2014), Ulyanovsk Region (Churakov et al., 2018), and
Novosibirsk Region (Tomoshevich, 2015). Thus, based
on the species composition of the regional dendroflo-
ra, we can assume that the species composition of Ery-
siphaceae on woody plants in Sverdlovsk Region has
been studied quite completely.
However, we should note that several more Erysi-
phaceae species on woody plants in Sverdlovsk Region
with a high degree of probability can be found, as they
are recorded in the neighboring regions in similar bi-
omes on the woody host plants, and are common fungi
in the whole middle Urals: Erysiphe prunastri DC.
(= Uncinula prunastri Sacc.) – was recorded in Chely-
abinsk Region on Prunus padus (Stepanova, Sirko,
1970), and three other species: Erysiphe penicillata
(Wallr.) Link [= Microsphaera alni (DC.) G. Winter]
on Alnus incana, Phyllactinia mali (Duby) U. Braun
[= Ph. suffulta (Rebent.) Sacc. f. oxyacanthae Roum.]
on Crataegus sanguinea, and Podosphaera aucupariae
Erikss. (= Р. o x ya c a n t h ae De Вагу f. sorbi Jacz.) on
Sorbus aucuparia L. – were found in Republic of Ba-
shkortostan (Yachevsky, 1927). Potentially, two addi-
tional ‘cryptic species’ would be found in Sverdlovsk
Region: Erysiphe syringae Schwein. – hardly differen-
tiated from E. syringae-japonicae by conidial stage
(Takamatsu et al., 2016), and E. hypophylla (Nevod.)
U. Braun et Cunningt. – hardly differentiated from
E. alphitoides by chasmothecia (Braun, Cook, 2012).
Phenological observations have shown that the de-
velopment of almost all powdery mildew fungi occurs
mainly in the period from mid-June to the end of Sep-
tember. Moreover, most species regularly formed chas-
mothecia (teleomorph, or sexual stage), and only four
species developed exclusively in the asexual stage (ana-
morph): Erysiphe aquilegiae, E. necator, Podosphaera
pannosa, and P. spiraeae; some other species: Erysiphe
alphitoides, E. syringae-japonicae, E. lonicerae, E. trifo-
liorum, Podosphaera aphanis, and Sawadaea bicornis
formed chasmothecia extremely rarely. Just all species
formed chasmothecia (teleomorph) mainly since the
mid-July to the mid-September.
The identified species are found on 49 species of
woody plants from 24 genera and 15 families, among
which the largest number of species was noted on the
species of Betulaceae, Rosaceae and Salicaceae (table
1). Each woody plant can be infected by a single pow-
dery mildew species, excluding Acer, Betula, Corylus,
Lonicera, and Salix, which can be infected with two
Erysiphaceae species (table 1). Three woody plant spe-
cies known as host plants for two Erysiphaceae species:
Acer platanoides (Sawadaea bicornis and S. tulasnei),
Betula pubescens (Erysiphe ornata and Phyllactinia be-
tulae), and Corylus avellana (Erysiphe cor ylacearum
and Phyllactinia guttata s. str.).
As our observations have shown, at least 14 species
(48.3%, or almost a half of known species) can be con-
sidered as alien for the region, including seven invasive
species that have come mainly from North America
(mainly United Stated of America): Erysiphe necator
and Podosphaera mors-uvae, and East Asia, including
Northeast China, Korea, Japan, and Russian Far East:
Erysiphe alphitoides, E. corylacearum, E. palczewskii,
E. syringae-japonicae, and E. vanbruntiana (Desprez-
Loustau, 2009; Braun, Cook, 2012). All of them are the
most common and harmful plant pathogens having a
high annual disease incidence and disease severity, sig-
nificantly reducing the decorative effect of their host
plants in Ekaterinburg. Also all of them have invaded
the region (as well as many European countries) over
the last century. Only three alien powdery mildew spe-
cies were known in Ekaterinburg (Sverdlovsk) before
1970 (Stepanova, Sirko, 1970): Erysiphe necator
since 1900s (Yachevsky, 1927), Podosphaera mors-uvae
– since 1910s (Yachevsky, 1927), and E. alphitoides
since 1920s (Pentin, 1939). Other four new recorded
East Asian alien species (previously reliably not record-
ed in Sverdlovsk and in the Urals) have invaded the re-
gion during the last 50 years (1971–2021): Erysiphe
vanbruntiana in 1970s (Gorlenko, Heluta, 1984),
E. palczewskii in 1980s (Heluta, 1981), E. syringae-ja-
328
МИКОЛОГИЯ И ФИТОПАТОЛОГИЯ том 56 № 5 2022
BULGAKOV, SHIRYAEV
ponicae in 1990s (Seko et al., 2008), and E. cory-
lacearum in 2010s (Bradshaw et al., 2021b) – all of
them are invasive species that spread in Europe during
the same periods.
Seven powdery mildews can be considered as alien
introduced species: Erysiphe berberidis, E. ehrenbergii,
E. euonymi, E. lonicerae, E. viburni, Podosphaera spi-
raeae, Sawadaea bicornis, and S. tulasnei – this species
are native for Eurasia (Braun, Cooke, 2012) and known
in European Russia (Gorlenko, 1983), Kazakhstan
(Rakhimova et al., 2015), and even Southwestern Urals
(Stepanova, Sirko, 1970). However, their appearance
in Sverdlovsk Region may be a consequence of their
host plant invasion in local plant communities (Sawa-
daea bicornis on Acer negundo), or introduction and ex-
panded cultivation of their host plants in regional ur-
ban plantings and private gardens (other powdery mil-
dews). All of the above-mentioned invasive species are
widespread and significantly reduce the decorative ef-
fect of their host plants in Ekaterinburg. It should be
noted that all these alien species originate from East or
Southeast Asia (Braun, Cook, 2012); they are known as
native species in the Russian Far East (mainly Pri-
morsky and Khabarovsk regions), China, Korea, and
Japan (Farr, Rossman, 2022).
We should note the first record of Erysiphe cory-
lacearum in the territory of Sverdlovsk Region, which
was first found in Ekaterinburg in 2021. This invasive
species have come from the East Asia near 2010, and
quickly spread throughout the habitat of hazels (Cory-
lus spp.) in the North America, Europe and West Asia,
including Asia Minor, the Caucasus, and Iran (Brad-
shaw et al., 2021). This harmful hazel pathogen was
first recorded in Russia on the Black Sea coast of the
Krasnodar region in 2013 (Bulgakov, 2018), and by
2016–2017 was found in other regions of Southern Euro-
pean Russia: the rest part of the Krasnodar region, in
the Crimea and Rostov region (Bulgakov, Karpun,
2020), and in Ukraine (Heluta, 2019) and Donetsk
People’s Republic (Bondarenko-Borisova, Bulgakov,
2019). T he discover y of E. corylacearum in Ekaterin-
burg can be considered as evidence that this species has
Table 1. Woody plants as hosts of the powdery mildews (Erysiphaceae) in Sverdlovsk Region
Host plants
Recorded fungal species, number
Families Genera Species (hybrids), number
Berberidaceae Berberis 21
Betulaceae Alnus 21
Betula 22
Corylus 12
Celastraceae Euonymus 11
Caprifoliaceae Lonicera 32
Ericaceae Vaccinium 11
Fabaceae Caragana 11
Chamaecytisus 11
Fagaceae Quercus 11
Grossulariaceae Ribes 31
Oleaceae Syringa 31
Ranunculaceae Clematis 21
Rosaceae Crataegus 21
Dasiphora 21
Prunus 11
Rosa 31
Spiraea 31
Salicaceae Populus 4 (2) 1
Salix 32
Sapindaceae Acer 32
Viburnaceae Sambucus 21
Viburnum 11
Vitaceae Vitis 21
Total: 15 24 49 (2) 29
МИКОЛОГИЯ И ФИТОПАТОЛОГИЯ том 56 № 5 2022
POWDERY MILDEWS (ERYSIPHACEAE) ON WOODY PLANTS 329
now spread throughout European Russia within the
range of common hazel (Corylus avellana L.) and entered
in Asian Russia throw Urals. The growth of Erysiphe
corylacearum on affected host plants leads to deforma-
tion of young leaves and shoots, and worsens the phy-
tosanitary condition of the hazel.
The research was supported by Russian Science
Foundation (project № 22-26-00228).
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Мучнисторосяные грибы (Erysiphaceae) на древесных растениях в городских
местообитаниях Свердловской области (Россия)
Т. С. Булгаков1,#, А. Г. Ширяев2,##
1 Институт экологии растений и животных УрО РАН, Екатеринбург, Россия
2 Субтропический научный центр Российской академии наук, Сочи, Россия
#e-mail: ascomycologist@yandex.com
##e-mail: anton.g.shiryaev@gmail.com
По результатам авторских исследований и ревизии предыдущих сведений установлен современный ви-
довой состав и составлен первый аннотированный список мучнисторосяных грибов на древесных рас-
тениях в городских местообитаниях Свердловской обл. (г. Екатеринбурга и нескольких городов обла-
сти). Всего в настоящее время выявлено 29 видов Erysiphaceae, среди которых большинство относится
к роду Erysiphe (17 видов), а остальные распределяются между родами Podospha era (7), Phyllactinia (3) и
Sawadaea (2). Шесть видов выявлены в Свердловской обл. впервые: Erysiphe ehrenbergii, E. euonymi,
E. lonicerae, E. viburni, Podosphaera myrtillina, and P. spiraeae. Почти половина всех выявленных видов
(14 из 29) являются чужеродными для Свердловской обл., при этом 6 видов могут рассматриваться как
инвазивные, из которых 2 вида происходят из Северной Америки (Erysiphe necator and Podos phaera
mors-uvae) и 4 вида – из Восточной Азии (Erysiphe alphitoides, E. corylacearum, E. palczewskii, and E. van-
bruntiana), а еще 8 видов могут рассматриваться как непреднамеренно интродуцированные из соседних
регионов вместе с их растениями-хозяевами. Развитие большинства отмеченных видов Er ysiphaceae
приходится на период с середины июня до конца сентября. Большинство видов (25 из 29) развиваются
как в стадии анаморфы, так и телеоморфы, и только 4 вида (Erysiphe aquilegiae, E. necator, Podosphaera
pannosa и P. spiraeae) отмечены исключительно в стадии анаморфы.
Ключевые слова: биоразнообразие грибов, городские насаждения, Россия, Урал, чужеродные виды
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