Additions to the knowledge of foliicolous micromycetes in Turkey

Abstract

Among microfungi collected on foliar spots of vascular plants in Yedigöller National Park, Bolu Province, Turkey, five species represent new records for Turkey: Ascochyta daturae, A. euonymi , Mycosphaerella laureolae , Phyllosticta datiscae, and Rhabdospora visci. Detailed descriptions and photographs of these species are provided.

Full text

MYCOTAXON
ISSN (print) 0093-4666 (online) 2154-8889 Mycotaxon, Ltd. ©2021
October–December 2021—Volume 136, pp. 841–852
https://doi.org/10.5248/136.841
Five new foliicolous micromycete records from Turkey
G D, M E*, Z A,
A I K, Z S, T E
1Graduate School of Natural and Applied Science,
Kırşehir Ahi Evran University, Bağbaşı, Kırşehir, Turkey
2Department of Landscape Architects, Faculty of Agriculture,
Kırşehir Ahi Evran University, Bağbaşı, Kırşehir, Turkey
3Department of Biology, Faculty of Science, Gazi University,
Teknikokullar, Ankara, Turkey
* C : merdogdu@ahievran.edu.tr
A—Among microfungi collected on foliar spots of vascular plants in Yedigöller
National Park, Bolu Province, Turkey, ve species represent new records for Turkey: Ascochyta
daturae, A. euonymi, Mycosphaerella laureolae, Phyllosticta datiscae, and Rhabdospora visci.
Detailed descriptions and photographs of these species are provided.
K —Ascomycota, biodiversity, new host, SEM, taxonomy
Introduction
Microfungi can cause various diseases through leaf infection. Ascochyta
Lib., Mycosphaerella Johanson, Phyllosticta Pers., and Rhabdospora (Durieu
& Mont.) Sacc. are among the genera that include species causing foliar
spots. Some of these foliar-pathogenic fungi show host specicity, while
others can be found on several hosts: e.g., Rhabdospora visci infects only
Viscum album, while Ascochyta daturae is observed on more than one
species in Solanaceae.
Foliar pathogens causing needle or leaf-bound diseases can cause growth
reduction as a result of a decrease in photosynthetic capacity at high levels of
infection (Van der Pas 1981, Manter & al. 2003, Hanso & Drenkhan 2012).

842 ... Doğan & al.
Tree mortality can be seen only in serious cases. By weakening the tree, leaf
diseases can contribute to higher sensitivity to biotic and abiotic stresses
(Bednářová & al. 2013, Kowalski 2013). Based upon trophic interactions
with the host, dierent pathogen species can be distinguished; for instance,
while necrotrophic fungi live on dead cells, biotrophic fungi directly derive
carbon and nutrients from living cells (Deacon 1997).
e Yedigöller National Park, located in the northern part of Bolu
Province in the Western Black Sea Region in Turkey, includes seven lakes
and many streams. e park is situated in square A3 of the Davis (1965–
85) grid square system. e climate of the province is oceanic, and it rains
during all seasons.
e research area comprises primarily mixed forest vegetation. At
lower elevations the forest is dominated by Fagus orientalis, Carpinus
orientalis, Quercus spp., Sambucus nigra, Sorbus aucuparia, S. torminalis,
Corylus colurna, Acer campestre, A. platanoides, Cornus mas, Populus
tremula, and Alnus glutinosa. Regions at upper elevations are covered with
Gymnospermae such as Abies nordmanniana subsp. equi-trojani, Pinus
nigra, P. sylvestris, and Taxus baccata. e understory contains shrubs such
as Daphne pontica, Rhododendron ponticum, and Juniperus oxycedrus. e
research area is also rich in marshy habitats, and there are aquatic plants in
the lake (e.g., Potamageton sp., Lemna sp.) and marsh plants surround the
edge of the lake (Typh a sp., Carex spp., Lythr um sp.).
Materials & methods
Plant specimens infected with microfungi were collected in the Yedigöller
National Park, Bolu Province, Turkey. Host specimens were prepared following
conventional herbarium techniques. Host plants were identied using the F
 T  E A I (Davis 1965–85). in sections prepared
from infected host tissue were examined under a Leica DM E light microscope and
measured from mounts in tap water. Twenty microscopic structures were measured
for each sample. Infected host surfaces were photographed using a Leica EZ4D stereo
microscope. Species were identied using relevant literature (Ascochyta: Vanev
& al. 1997, Mel’nik 2000, Połeć & Ruszkiewicz-Michalska 2011; Mycosphaerella:
Ciferri 1956; Phyllosticta: Sydow 1899, Cejp 1965; Rhabdospora: Winter 1883 [as
Septoria], Saccardo 1884 [as Septoria], Diedicke 1914). All examined specimens
were deposited in the Mycological Collection of the Department of Landscape
Architects, Faculty of Agriculture, Kırehir Ahi Evran University, Kırehir, Turkey
(AEUT).

Microfungal foliar pathogens new to Turkey ... 843
F. 1. Ascochyta daturae (AEUT GD1376). A. leaf spot (detail) showing pycnidia; B. pycnidia on
leaf (SEM); C. pycnidium, vertical section; D, E. conidia; F. conidium (SEM).
For scanning electron microscopy (SEM), infected leaves were mounted on
stubs with double-sided tapes. ey were coated with gold in Polaron SC 502
Sputter Coater and examined with Jeol JSM 6060 SEM at 5‒10 kV in the Faculty of
Science, Gazi University, Ankara, Turkey.
Taxonomy
During our study on microfungi on vascular plants in Yedigöller National
Park in Turkey we collected several microfungal species that cause foliar

844 ... Doğan & al.
spots. A check of the current literature revealed that among the microfungal
species causing foliar spots determined in this study, Ascochyta daturae,
Ascochyta euonymi, Mycosphaerella laureolae, Phyllosticta datiscae, and
Rhabdospora visci represent new records for Turkey. e list of microfungi
with their descriptions, host plants, habitats, localities, collection dates, and
voucher numbers follow the classication provided by Index Fungorum
(2020) with slight modications.
Ascochyta daturae Sacc., Michelia 1(2): 163 (1878) F. 
S visible on both sides of leaves, generally circular or angular,
5–15 mm diam., sometimes elongated 23–45 × 12–15 mm, pale brown,
margin of spots dark brown. C pycnidial, epiphyllous,
aggregated or scattered, unilocular, globose, globose-depressed, semi-
immersed, 100–190 × 85–140 µm, light brown; ostiole circular or sometimes
papillate, 25–30 µm diam. C cylindrical, oblong, ellipsoid, 1-septate,
rarely aseptate, straight or slightly curved, not or slightly constricted, both
ends rounded, sometimes one end slightly narrowed, 6.4–11 × 2.8–4 µm,
guttulate, hyaline.
S —TURKEY, B P: Yedigöller National Park, near the
Büyük Lake, 40°56′28″N 31°44′51″E, 770 m asl, on living leaves of Atropa belladonna L.
(Solanaceae), 28.06.2018, G. Doğan (AEUT GD1376).
D—Bulgaria (Vanev & al. 1997); Canada (Ginns 1986); China
(Tai 1979); Poland (Mulenko & al. 2008); Venezuela (Urtiaga 1986).
N: Ascochyta consists of facultative parasites that cause diseases
of many cultivated and wild plants. A few species are known only from
dead parts of their host plants (Mel’nik 2000). In Turkey, Ascochyta
species are poorly known and not yet intensively studied. Some species
of Ascochyta were reported by Bremer & al. (1947, 1948), Karel (1958),
Göbelez (1964), Parlak & Gucin (1993), Eken (2003), and Kabaktepe &
al. (2019). Bahçecioğlu & Kabaktepe (2013) listed 20 Ascochyta species
from Turkey, on 25 plant species (in 21 genera and 16 families). Mel’nik
(2000) synonymised A. atropae Bres. (the only species recorded on Atropa
belladonna) with A. daturae, which has been recorded on living and dry
leaves and other parts of members of Solanaceae. Microscopic features of
our specimen corresponded to those given by Mel’nik (2000) and Połeć &
Ruszkiewicz-Michalska (2011). We observed unicellular conidia on our
specimens similar to those reported by Połeć & Ruszkiewicz-Michalska
(2011).

Microfungal foliar pathogens new to Turkey ... 845
F. 2. Ascochyta euonymi (AEUT GD1980). A. leaf spots; B, C. pycnidia on leaf (SEM);
D. pycnidium, vertical section; E. conidia; F. conidia (SEM).
Ascochyta euonymi Pass., Diagn. Funghi Nuovi 5: 11 (1891) F. 
S visible on both sides of leaves, mostly circular, 10–15 mm diam.,
whitish, surrounded by a brown border. C pycnidial, epiphyllous,
scattered, unilocular, globose, semi-immersed, 60–115 µm diam., brown;
ostiole papillate, 27–40 µm diam. C cylindrical, ellipsoid, lanceolate,
straight, aseptate or 1-septate, not constricted, both ends rounded, sometimes
one end slightly narrowed, 3.8–6.8 × 2–3 µm, guttulate, hyaline.

846 ... Doğan & al.
S —TURKEY, BOLU: Yedigöller National Park, 40°53′45″N,
31°40′06″E, 1627 m asl, on living leaves of Euonymus verrucosus Scop. (Celastraceae),
02.08.2019, G. Doğan (AEUT GD1980).
D—Czechoslovakia (Farr & Rossman 2020); Georgia
(Nakhutsrishvili 1986); Italy (Mel’nik 2000).
N: Ascochyta euonymi, A. euonymella (Sacc.) Allesch., A. euonymicola
Allesch., and A. oudemansii Sacc. & P. Syd. are reported to infect Euonymus
spp. (Mulenko & al. 2008, Mel’nik 2000). Our specimen is morphologically
similar to Ascochyta euonymi as described by previous study (Mel’nik 2000),
but diers in having slightly broader, shorter, 1–2-celled conidia.
Mycosphaerella laureolae (Desm.) Lindau,
Nat. Panzenfam. 1(1): 424 (1897) F. 3
S single or conuent, amphigenous, usually circular, irregular
when conuent, 5–11 mm diam., at rst blackish, becoming brown in the
centre, surrrounded by a dark ring. P mostly epiphyllous, rarely
hypophyllous, usually grouped in the centre of the spots, globose, 65–100
µm diam., blackish; ostiole papillate, 18–20 µm diam. A bitunicate,
subcylindric to clavate, attenuate at the base, contracted almost stipitate,
33–50 × 8–10.7 µm. A biseriate, oblong, ovate or ellipsoid,
1-septate, straight, not constricted, both ends rounded, 12.4–15.8 × 3.6–4.7
µm, guttulate, hyaline.
S —TURKEY, B P: Yedigöller National Park, Mengen
road separation, 40°56′38″N 31°44′51″E, 741 m asl, on living leaves of Daphne pontica
L. (ymelaeaceae), 03.05.2019, G. Doğan (AEUT GD1792).
D—Dominican Republic (Ciferri 1956); France, Germany, and
Switzerland (Stevenson 1926); Morocco (Rieuf 1970, as Sphaerella laureolae).
N: Mycosphaerella s.lat. is one of the largest groups of ascomycetes
and includes more than 3000 taxa, with species recognized as pathogens or
endophytes of many plants, hyperparasites of other fungi, or saprobes (Crous
2009). Our identication of Mycosphaerella laureolae agrees with other
descriptions of the species with respect to the morphology of perithecia, asci,
and ascospores, the only observable dierence being the wider dimensions
of ascospores and the smaller dimensions of asci. Ciferri (1956) described
ascospores measuring 10–15 × 2–3 µm and asci measuring 40–50 × 8–10 µm;
and Saccardo (1882) described ascospores measuring 12–14 × 3 µm and asci
measuring 44 × 8 µm (as Sphaerella laureolae). Here we report Daphne pontica
as a new host for Mycosphaerella laureolae.

Microfungal foliar pathogens new to Turkey ... 847
F. 3. Mycosphaerella laureolae (AEUT GD1792). A. leaf spot (detail) showing perithecia;
B. perithecia on leaf (SEM); C. perithecium on leaf (SEM); D. perithecium, vertical section;
E. ascus and ascospores; F, G. ascospores mounted in lactophenol cotton blue.
Phyllosticta datiscae P. Syd., Beibl. Hedwigia 38: (135) (1899) F. 
S amphigenous, orbicular to oblong, oen with concentric rings,
reaching a diam. of about 1 cm, brown, margin of spots dark brown.
C pycnidial, epiphyllous, scattered, unilocular, globose-depressed,
semi-immersed, 110–135 × 70–100 µm, brown; ostiole papillate. C
one-celled, oblong, ellipsoid, rounded at both ends, 5.5–6.9 × 2.2–2.7 µm,
biguttulate, hyaline.

848 ... Doğan & al.
F. 4. Phyllosticta datiscae (AEUT GD2041). A. leaf spot (detail) showing pycnidia;
B. pycnidium, vertical section; C. conidia; D. conidia (SEM).
S —TURKEY, B P: Yedigöller National Park,
40°56′52″N 31°45′02″E, 716 m asl, on living leaves of Datisca cannabina L. (Datiscaceae),
27.06.2018, G. Doğan (AEUT GD1328); Mengen road separation, 40°56′30″N
31°44′40″E, 811 m asl, on living leaves of Datisca cannabina, 03.08.2019, G. Doğan
(AEUT GD2041).
D—Germany (Sydow 1899), Czechoslovakia (Cejp 1965).
N: Phyllosticta is an important genus of plant pathogenic fungi, causing
leaf spots and various fruit diseases worldwide on a large range of hosts (Aa
& Vanev 2002). Species recognition in Phyllosticta has historically been based
on morphology, culture characters, and host association. Although there have
been several taxonomic revisions and enumerations of species, there is still
considerable confusion when identifying taxa (Wikee & al. 2011). Phyllosticta
datiscae is the only species of Phyllosticta described on Datisca cannabina. e
Turkish specimens agree with the description by Sydow (1899) in leaf spot,
conidiomatal, and conidial morphology, except that the conidiomata are larger
and the conidia smaller; in comparison with the description and illustration by
Cejp (1965), the Turkish conidia were thicker and 1–2-celled.

Microfungal foliar pathogens new to Turkey ... 849
F. 5. Rhabdospora visci (AEUT GD 2014). A. leaf spot (detail) showing perithecia;
B. perithecium, vertical section; C. conidia; D. ascospores mounted in lactophenol cotton blue;
E, F. conidia (SEM).
Rhabdospora visci (Bres.) Died.,
Krypt.. Brandenburg 9(3): 537 (1914 [“1915”] F. 5
L  amphigenous, raised, circular, 2–4 mm diam. or conuent and
larger, pale brown, surrounded by a reddish-brown border. C
pycnidial, mostly hypophyllous, scattered or in groups, unilocular,
subglobose, immersed, later becoming erumpent, 175–350 µm diam., dark
brown. C liform, straight or slightly curved, 1–3-septate, non-

850 ... Doğan & al.
constricted at the septum, attenuated both ends, (18.5–)24.6–36 × 2.2–2.9
µm, guttulate, hyaline.
S —TURKEY, B P: Yedigöller National Park,
40°93′58″N 31°75′39″E, 1083 m asl, on living leaves of Viscum album subsp. abietis
(Wiesb.) Abrom. (Santalaceae), 02.08.2019, G. Doğan (AEUT GD 2014).
D—Austria/Italy (Winter 1883, as Septoria visci); Germany
(Diedicke 1914); Hungary (Geza & al. 2009, as Septoria visci); Italy (Farr
& Rossman 2020, as Septoria visci); Serbia and Bosnia and Herzegovina
(Stanivuković & al. 2010, as Septoria visci).
N: Biological control of parasites by using plant pathogens has gained
acceptance as a practical, safe and environmentally benecial management
method applicable to agro-ecosystems (Charudattan 2001). Control of
European mistletoe is a major problem for the forest service in Turkey (Yüksel
& al. 2005). More than 20 microscopic fungi live on European mistletoe, but
only a few of them cause major damage on the plant (Karadžić & al. 2004).
Of these, Rhabdospora visci, which causes leaf spot disease of European
mistletoe, appears to have potential as a biological control agent against of this
semiparasite.
is species was initially described as Septoria visci on leaves of Viscum
album parasitising gymosperm trees in South Tyrol (Winter 1883). It was
later transferred to the genus Rhabdospora by Diedicke (1914). Our specimen
of Rhabdospora visci was morphologically similar to specimens described by
previous studies (Winter 1883, Diedicke 1914) but diered in having slightly
thicker and shorter conidia.
Acknowledgments
e authors thank Meike Piepenbring (Goethe University, Frankfurt am
Main) and Sabeena Aliyarukunju (Jawaharlal Nehru Tropical Botanic Garden and
Research Institute, India) for pre-submission review. is work was supported by
the Scientic and Technological Research Council of Turkey (TÜBİTAK) (Project
No: 217Z038).
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