And Typification of Paragnomonia Fragariae, the Cause of Strawberry
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Fungal Biology 123 (2019) 791e803 Contents lists available at ScienceDirect Fungal Biology journal homepage: www.elsevier.com/locate/funbio Reassessment of Paragnomonia (Sydowiellaceae, Diaporthales) and typification of Paragnomonia fragariae, the cause of strawberry root rot and petiole blight * Inga Morocko-Bicevska a, , Jamshid Fatehi a, b, Olga Sokolova a a Institute of Horticulture, Graudu str. 1, Dobele, LV, 3701, Latvia b Lantmannen€ BioAgri, Fågelbacksvagen€ 3, SE-756 51, Uppsala, Sweden article info abstract Article history: Paragnomonia fragariae is a plant pathogenic ascomycete causing root rot and petiole blight of perennial Received 25 February 2019 strawberry in northern Europe. This paper provides a revised description of Paragnomonia and P. fra- Received in revised form gariae with lecto- and epitypification based on the species original description, recent collections from 31 July 2019 four European countries, examination of specimens used in the previous taxonomic studies and Accepted 5 August 2019 phylogenetic analyses of DNA sequences of LSU, ITS/5.8S and tef1-a. This study presents the first report of Available online 15 August 2019 P. fragariae on cultivated strawberry in Finland and Lithuania. Our study on growth rate showed that P. Corresponding Editor: J Slot fragariae is a cold-adapted fungus growing almost equally at 5 Casat20C and attaining maximal growth at 15 C. New primers were designed for amplification of ca. 0.8 kb fragment of tef1-a of Sydo- Keywords: wiella fenestrans. Additionally, newly generated sequences of tef1-a were obtained for the first time from Epitype 21 isolates of seven species belonging to five genera of Sydowiellaceae, including the type species S. ITS fenestrans, therefore considerably contributing to the current knowledge on phylogenetic relationships of Lectotype this insufficiently studied group of fungi. The phylogenetic analysis has also revealed that the recently LSU described species “S.” centaureii is genetically distant from the generic type S. fenestrans and other Molecular phylogeny Sydowiella. Translation elongation factor 1-a © 2019 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 1. Introduction fructicola (G. Arnaud) Fall) by misusing the name Gnomonia fra- gariae Kleb. for the specimens of Gnomonia comari P. Karst sensu Paragnomonia fragariae, initially discovered by Klebahn (1918) lato (Alexopoulos and Cation, 1952; Parikka, 1981; CMI Distribution and described as Gnomonia fragariae, is a plant pathogen causing maps of plant diseases, No. 438, 1982). This taxonomical confusion severe root rot and petiole blight of perennial strawberry in has already been notified by several authors (Bolay, 1972; Maas, northern Europe (Morocko et al., 2006; Morocko-Bicevska and 1998; Farr et al., 1989; Morocko and Fatehi, 2007; Sogonov et al., Fatehi, 2011). So far, the fungus has undoubtedly been reported 2008; Walker et al., 2010). G. fructicola occurs worldwide on from Germany, Latvia, Sweden, Switzerland, and the United strawberry causing leaf blotch, fruit rot, petiole blight, stem end rot Kingdom (Kelabhn, 1918; Bolay, 1972; Morocko, 2006; Morocko and root rot particularly in synergic interaction with nematodes et al., 2006). Besides cultivated strawberry, the fungus also has (Alexopoulos and Cation, 1948; Shipton, 1967; Bolay, 1972; Kurppa been found on wild species of Fragaria and Potentilla in Switzerland and Vrain, 1989; Gubler and Feliciano, 1999; Sogonov et al., 2008). (Bolay, 1972). Since the first discovery of P. fragariae in 1918, the The taxonomy of G. fructicola was studied and resolved by Sogonov identity of this fungus has been confused in several studies with the et al. (2008) and Walker et al. (2010). another strawberry pathogen Gnomoniopsis fructicola (G. Arnaud) The genus Gnomonia and families in Diaporthales have been the Sogonov (syn. Gnomonia fragariae f. fructicola G. Arnaud; Gnomonia subject of detailed morphological and molecular studies over the last decade (Sogonov et al., 2008; Crous et al., 2012; Kruys and Castlebury, 2012; Voglmayr et al., 2012; Walker et al., 2012; Voglmayr and Jaklitsch, 2014; Suetrong et al., 2015; * Corresponding author. Norphanphoun et al., 2016; Du et al., 2017; Senanayake et al., E-mail addresses: [email protected] (I. Morocko-Bicevska), Jamshid.Fatehi@ lantmannen.com (J. Fatehi), [email protected] (O. Sokolova). 2017a; b; Voglmayr et al., 2017). The new concept of Gnomonia https://doi.org/10.1016/j.funbio.2019.08.002 1878-6146/© 2019 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 792 I. Morocko-Bicevska et al. / Fungal Biology 123 (2019) 791e803 has reduced the number of accepted species from 280 to only a few For morphological examination of the fungus in culture, the isolates species sharing common phylogenetic, morphological and host were grown on OA, PCA, and PDA plates incubated at room tem- characteristic features (Sogonov et al., 2008). Our previous study on perature on a laboratory bench exposed to natural light or in a molecular characterisation of P. fragariae demonstrated that the growth chamber at 22 C with 12 h daily illumination of cool-white genus Gnomonia was polyphyletic and P. fragariae was genetically (Osram L 15W/840) lamps for at least four weeks. Optimal growth distant from the type species of Gnomonia, G. gnomon, and other temperature of P. fragariae was determined for four isolates S1, S4, members of family Gnomoniaceae (Morocko and Fatehi, 2007). M1 and UN35 grown in two replicates (plates) on PDA, PCA, corn Moreover, the phylogeny of Diaporthales inferred from rDNA se- meal agar (CMA, Difco), and water agar (WA) at temperature re- quences showed that P. fragariae belonged to Sydowiellaceae,a gimes from 5 e 30 C with 5 C intervals in the dark. The agar plates family harbouring genera with diverse morphology, host range and were inoculated with five mm in diameter plugs of actively growing habitat (Rossman et al., 2007; Kruys and Castlebury, 2012). fungal cultures. The growth was measured daily along two In a recent study by Senanayake et al. (2017b), on the basis of perpendicular lines drawn at the centre of the colonies and previously published rDNA sequences (Morocko and Fatehi, 2007), continued for two weeks. and apparently some morphological interpretations inferred from The list of fungal isolates studied, the culture and voucher the literature related to P. fragariae or G. fructicola (Alexopoulos and numbers, hosts, collection data and GenBank accession numbers of Citation, 1952; Morocko and Fatehi, 2007), a monotypic genus DNA sequences obtained in this study or extracted from the Gen- Paragnomonia Senan. & K.D. Hyde in Sydowiellaceae and a new Bank are provided in Table 1. Details of specimens used for combination P. fragariae (Kleb.) Senan. & K.D. Hyde were intro- morphological examinations are listed in the Taxonomy section. duced to replace G. fragariae Kleb. However, several of the The living fungal cultures are maintained at the microbial strain morphological characters presented by the authors in the new collection at the Institute of Horticulture, Dobele, Latvia. Repre- description of P. fragariae were incorrect and repetitive of those sentative isolates of the studied fungi were deposited in the Mi- previous taxonomic confusions surrounding P. fragariae and G. crobial strain collection of Latvia (MSCL), Riga, Latvia and fructicola. The main misperception is the attribution of an asexual Westerdijk Fungal Biodiversity Centre (CBS-KNAW), Utrecht, The morph for P. fragariae that has never been observed or reported by Netherlands. The dry specimens were deposited in the Herbarium any of the authors who have extensively examined and studied P. of University of Daugavpils (DAU), Daugavpils, Latvia and Swedish fragariae specimens and isolates on host plants and living cultures Museum of Natural History (S), Stockholm, Sweden. (Klebahn, 1918; Bolay, 1972; Monod, 1983; Morocko and Fatehi, 2007). In addition, characteristics and measurements of asci and 2.2. DNA extraction, PCR amplification and sequencing ascospores do not correspond to those described by Klebahn (1918) and other authors dealing with P. fragariae (Bolay, 1972; Monod, Fungal mycelium preparations, DNA extraction, and amplifica- 1983; Morocko and Fatehi, 2007), but they agree more with G. tion of partial nuLSU and entire ITS1-5.8S-ITS2 rDNA regions were fructicola (Walker et al., 2010). Moreover, P. fragariae does not form carried out as described previously (Morocko and Fatehi, 2007), ascomata on roots in nature, but only on petioles because it requires with an exception that REDTaq® ReadyMix™ PCR reaction mix light for sporulation either on host tissues or agar media (Morocko (SigmaeAldrich) was used in PCR amplification. and Fatehi, 2007). Approximately 1.0 kb fragment of translation elongation factor 1 In a present study, we reassess and provide the revised alpha (tef1-a) gene was amplified with primers EF1-728F (Carbone description of Paragnomonia and P. fragariae based on the original and Kohn, 1999) and EF1-1567R (Rehner, 2001). For Sydowiella description of the species by Klebahn (1918), examination of fenestrans ca. 0.8 kb fragment of tef1-a gene was amplified using specimens collected previously by other authors, our collection newly designed forward primer EF1-F12 (50 AGCTTGG- from four European countries, and phylogeny of LSU, ITS/5.8S and CAAGGGTTCCTTCA 3’) and reverse primer EF1-1567R (Rehner, tef-1a gene sequences. We could not find the type specimens