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Host Range of Hymenoscyphus Fraxineus in Slovak Arboreta

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Host Range of Hymenoscyphus Fraxineus in Slovak Arboreta Article Host Range of Hymenoscyphus fraxineus in Slovak Arboreta Katarína Pastirˇcáková 1,* , Katarína Adamˇcíková 1, Marek Barta 1 , Jozef Pažitný 1, Peter Hot’ka 2, Ivana Sarvašová 3 and Miriam Kádasi Horáková 1 1 Department of Plant Pathology and Mycology, Institute of Forest Ecology, Slovak Academy of Sciences, Akademická 2, SK-94901 Nitra, Slovakia; [email protected] (K.A.); [email protected] (M.B.); [email protected] (J.P.); [email protected] (M.K.H.) 2 MlyˇnanyArboretum, Institute of Forest Ecology, Slovak Academy of Sciences, Vieska nad Žitavou 178, SK-95152 Slepˇcany, Slovakia; [email protected] 3 Borová Hora Arboretum, Technical University in Zvolen, Borovianska cesta 2171/66, SK-96053 Zvolen, Slovakia; [email protected] * Correspondence: [email protected] Received: 13 April 2020; Accepted: 22 May 2020; Published: 25 May 2020 Abstract: The health of 34 different Fraxinus taxa in association with the pathogenic fungus Hymenoscyphus fraxineus was assessed in four Slovak arboreta. Averaged across all arboreta, nearly one-quarter (24.9%) of all evaluated trees showed ash dieback symptoms. The damage was most serious on the common ash F. excelsior, a native species. The percentage of dead trees did not exceed 2% for all evaluated trees. Generally, ash trees of all ages were affected, though the intensity of the damage varied among the sites. The identity of H. fraxineus was confirmed by conventional PCR targeting the internal transcribed spacer (ITS) sequences of the nuclear ribosomal DNA, as well as the 18S gene/ITS-2 region of the rDNA operon. In Slovakia, the pathogen has expanded its host range from native species not only to their ornamental cultivars, but also to introduced North American (F. cinerea, F. latifolia, F. pennsylvanica, F. quadrangulata) and Asian (F. bungeana, F. chinensis ssp. rhynchophylla, F. mandshurica) ash species. H. fraxineus was also observed on the previous year’s leaf petioles of the native European species F. ornus, considered a weakly susceptible host. In Slovak arboreta, H. fraxineus was found on 23 Fraxinus taxa; 21 of them represent first records for the country. F. bungeana is recorded as a new host species of H. fraxineus. Keywords: ash dieback; crown defoliation; Fraxinus spp.; Hymenoscyphus fraxineus 1. Introduction Fraxinus L. (Oleaceae) is widely distributed over North and Central America, Asia, Europe, and Northwest Africa, from tropical to temperate climates [1]. Although Fraxinus often grows in forests, at their edges, and along tree-lined roads, it is also planted in urban greenery and parks as an ornamental tree. Since the early 1990s, ash dieback is a serious disease that has been killing ash across Europe [2–5]. The disease is caused by the invasive fungus Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz & Hosoya (syn. Hymenoscyphus pseudoalbidus Queloz, Grünig, Berndt, T. Kowalski, T.N. Sieber & Holdenr.), the anamorph of which is Chalara fraxinea T. Kowalski. Currently, it is one of seven known species of the genus Hymenoscyphus Gray (Helotiales) occurring on ash trees. The non-pathogenic species Hymenoscyphus albidus (Gillet) W. Phillips has been known from Europe since 1851 [6]. Gross and Han [7] and Gross et al. [8] described three Asian Hymenoscyphus species, H. koreanus A. Gross & J.G. Han, H. linearis Hosoya, A. Gross & Baral, and H. occultus A. Gross & J.G. Han. Although pathogenicity tests revealed that H. linearis is avirulent [8], there is currently no information on the pathogenicity of H. koreanus and H. occultus. Recently, Kowalski and Bilanski [9] have identified another species, H. pusillus T. Kowalski & P. Bila´nski, from F. pennsylvanica Marshall in Poland, but the pathogenicity of this fungus Forests 2020, 11, 596; doi:10.3390/f11050596 www.mdpi.com/journal/forests Forests 2020, 11, 596 2 of 18 has notForests yet been 2020, 11 confirmed., x FOR PEER REVIEWH. caudatus (P. Karst.) Dennis, occurring on various plant species,2 of 18 has also been recorded on ash in China [10] and the British Isles [11]. identified another species, H. pusillus T. Kowalski & P. Bilański, from F. pennsylvanica Marshall in H. fraxineus Poland, butis the widespread pathogenicity in bothof this East fungus Asia has (Northeastern not yet been China,confirmed. Japan, H. caudatus Korea, (P. and Karst.) the Russian Far East)Dennis, and Europeoccurring [12 on]. various In Europe, plant species, this pathogen has also been mainly recorded attacks on ash common in China [10] ash and (F. the excelsior British L.) and narrow-leavedIsles [11]. ash (F. angustifolia Vahl), but it is also recorded on North American (F. americana L., F. nigra Marshall,H. fraxineusF. pennsylvanica is widespread) in and both Asian East Asia (F.mandshurica (Northeastern Rupr.,China, Japan,F. sogdiana Korea,Bunge) and the Russian ash species in EstoniaFar [13 ,East)14]. H.and fraxineus Europe [12].has In been Europe, recorded this pathogen from F. ornusmainlyL. attacks onlyin common Austria ash [15 (F.]. excelsior In Danish L.) and arboretum, narrow-leaved ash (F. angustifolia Vahl), but it is also recorded on North American (F. americana L., F. H. fraxineus apothecia were equally well-formed on many introduced host Fraxinus species as it was on nigra Marshall, F. pennsylvanica) and Asian (F. mandshurica Rupr., F. sogdiana Bunge) ash species in commonEstonia ash [16 [13,14].]. Most H. recently,fraxineus thehas fungusbeen recorded has been from found F. ornus on threeL. only new in Austria oleaceous [15]. host In Danish plant species (Chionanthusarboretum, virginicus H. fraxineusL., Phillyrea apothecia angustifolia were equallyL., Phillyrea well-formed latifolia on manyL.) at introduced Westonbirt host Arboretum Fraxinus in the United Kingdomspecies as [it17 was]. These on common were the ash first [16]. findings Most recently, on hosts the other fungus than hasFraxinus been found. In Slovakia,on three new two native Europeanoleaceous ash species host plant (F. excelsior species (,ChionanthusF. angustifolia virginicus) are attackedL., Phillyrea by angustifoliaH. fraxineus L., Phillyrea[18–21 ].latifolia Previous L.) at papers have onlyWestonbirt recorded Arboretum ash dieback in the onUnited these Kingdom two native [17]. TheseFraxinus were speciesthe first findings in forest on stands, hosts other seed than orchards, Fraxinus. In Slovakia, two native European ash species (F. excelsior, F. angustifolia) are attacked by H. and tree alleys in Slovakia. The health of non-native ash trees and ornamental cultivars of native fraxineus [18–21]. Previous papers have only recorded ash dieback on these two native Fraxinus species,species however, in forest has stands, not yet seed been orchar investigatedds, and tree in alleys Slovakia. in Slovakia. The health of non-native ash trees Theand aims ornamental of this studycultivars were of native (i) to species, evaluate however, the health has not of yet introduced been investigated ash species in Slovakia. and ornamental cultivars ofThe native aimsFraxinus of this studyspecies were in(i) termsto evaluate of the the occurrencehealth of introduced of H. fraxineus ash speciesin and Slovak ornamental arboreta and (ii) to determinecultivars of the native host Fraxinus range species of H. fraxineus in terms ofin the the occurrence arboreta. of H. fraxineus in Slovak arboreta and (ii) to determine the host range of H. fraxineus in the arboreta. 2. Materials and Methods 2. Materials and Methods 2.1. Study Sites 2.1. Study Sites Study materialStudy material was collectedwas collected in threein three arboreta arboreta situated in in central central Slovakia Slovakia and one and arboretum one arboretum in in SouthwesternSouthwestern Slovakia Slovakia (Figure (Figure1, Table 1, Table1). 1). FigureFigure 1. Map 1. Map of of Slovakia Slovakia showingshowing the the four four sampled sampled arboreta. arboreta. The Borová Hora ArboretumTable 1. Characteristics(Zvolen District) ofis sp studyread sitesover inthe Slovakia. southwestern slopes of Zvolenská vrchovina upland, which is one of the geomorphological units of the Zvolenská kotlina basin; it is Total Area Altitude MAT MTGS APS MPSGS Arboretumcharacteristically upland. From a climaticCoordinates point of view, this area is warm and slightly humid (Figure [ha] [m a.s.l.] [◦C] [◦C] [mm] [mm] 2), with a cold winter [22]. BorováThehora Kysihýbel 47.80Arboretum 48 (Banská◦350 N 19Štiavnica◦080 E District) 291–377 is located 9.7 near 16.8 the town763.3 of Banská432.1 KysihŠtiavnica.ýbel The area is 7.78 protected 48by◦ the270 ŠtiavnicN 18◦56ké0 E vrchy 530–563 Mountains Protected 9.1 15.8Landscape853.3 Area. This465.8 Liptovskforestryý Hr arboretumádok is7.24 a unique experimental 49◦020 N 19 ◦forestry430 E area 641–646 specialized 8.0in rapidly 14.6 growing729.5 exotic wood460.2 Mlyˇnanyspecies [23]. It is in 67.00 a warm temperate 48◦190 N 18zone◦22 with0 E a 163–217humid climate 10.7 (Figure 17.5 2), without555.5 extreme337.0 MAT—meantemperature annual changes. temperature; MTGS—mean temperature in the growing season; APS—annual precipitation sum; MPSGS—mean precipitation sum in the growing season. The growing season is from April to September. The climatic data were computed for the ten-year period 2009–2018 (data source: Slovak Hydrometeorological Institute, Bratislava). Forests 2020, 11, x FOR PEER REVIEW 3 of 18 The Liptovský Hrádok Arboretum (Liptovský Mikuláš District) is situated in an urban area in the town of Liptovský Hrádok. This area has warm, humid summers and cold winters. The Liptovský Forests 2020, 11, 596 3 of 18 Hrádok Arboretum is the highest elevation arboretum in Central Europe and is registered as a protected area under the Nature and Landscape Protection Act of Parliament [24]. The BorovMlyňanyá Hora Arboretum Arboretum (Zlaté (Zvolen Moravce District) District) is spread is a overlarge the park southwestern situated in slopesone of ofthe Zvolensk warmestá vrchovinaand driest upland,areas of whichSlovakia is onein the of thesouthern geomorphological foothills of the units Carpathian of the Zvolensk Mountainsá kotlina at the basin; northern it is characteristicallyedge of the hottest upland.
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