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That Glitters Is Not Ramularia

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That Glitters Is Not Ramularia Accepted Manuscript All that glitters is not Ramularia S.I.R. Videira, J.Z. Groenewald, U. Braun, H.-D. Shin, P.W. Crous PII: S0166-0616(16)30001-X DOI: 10.1016/j.simyco.2016.06.001 Reference: SIMYCO 28 To appear in: Studies in Mycology Please cite this article as: Videira SIR, Groenewald JZ, Braun U, Shin H-D, Crous PW, All that glitters is not Ramularia, Studies in Mycology (2016), doi: 10.1016/j.simyco.2016.06.001. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT All that glitters is not Ramularia S.I.R. Videira 1,2, J.Z. Groenewald 1, U. Braun 3, H.-D. Shin 4, and P.W. Crous 1,2,5* 1CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT, Utrecht, the Netherlands ; 2Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands ; 3Martin-Luther-Universität, Institut für Biologie, Bereich Geobotanik und Botanischer Garten, Herbarium, Neuwerk 21, D-06099 Halle (Saale), Germany ; 4Division of Environmental Science and Ecological Engineering, Korea University, Seoul 02841, Korea ; 5Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria 0002, South Africa *Correspondence : Pedro W. Crous, [email protected] Abstract: Ramularia is a species-rich genus that harbours plant pathogens responsible for yield losses to many important crops, including barley, sugar beet and strawberry. Species of Ramularia are hyphomycetes with hyaline conidiophores and conidia with distinct, thickened, darkened, refractive conidiogenous loci and conidial hila, and Mycosphaerella sexual morphs. Because of its simple morphology and general lack of DNA data in public databases, several allied genera are frequently confused with Ramularia . In order to improve the delimitation of Ramularia from allied genera and the circumscription of species within the genus Ramularia , a polyphasic approach based on multilocus DNA sequences, morphological and cultural data were used in this study. A total of 420 isolates belonging to Ramularia and allied genera was targeted for the amplification and sequencing of six partial genes. Although Ramularia and Ramulariopsis proved to be monophyletic, Cercosporella and Pseudocercosporella were polyphyletic. Phacellium isolates clustered within the Ramularia clade and the genus is thus tentatively reduced to synonymy under Ramularia . Cercosporella and Pseudocercosporella isolates that were not congeneric with the ex-type strains of the type species of those genera were assigned to existing genera or to the newly introduced genera Teratoramularia and Xenoramularia , respectively. Teratoramularia is a genus with ramularia-like morphology belonging to the Teratosphaeriaceae, and Xenoramularia was introduced to accommodate hyphomycetous species closely related to Zymoseptoria . The genera Apseudocercosporella , Epicoleosporium , Filiella , Fusidiella , Neopseudocercosporella , and Mycosphaerelloides were also newly introduced to accommodate species non-congeneric with their purported types. A total of nine new combinations and 24 new species were introduced in this study. Key words: Barcoding, cercosporoid, multilocus phylogeny, Mycosphaerella , plant pathogen. Taxonomic novelties: New genera – Apseudocercosporella Videira & Crous, Epicoleosporium Videira & Crous, Filiella Videira & Crous, Fusoidiella Videira & Crous, Mycosphaerelloides Videira & Crous, Neopseudocercosporella Videira & Crous, Teratoramularia Videira, H. -D. Shin & Crous, Xenoramularia Videira, H. -D. Shin & Crous; New combinations – Filiella pastinacae (P. Karst.) Videira & Crous, Fusoidiella depressa (Berk. & Broome) Videira & Crous, Mycosphaerelloides madeirae (Crous & Denman) Videira & Crous, Neopseudocercosporella brassicae (Chevall.) Videira & Crous, Neopseudocercosporella capsellae (Ellis & Everh.) Videira & Crous, Ramularia cerastiicola (Crous) Videira & Crous, Ramularia stellariicola (M.J. Park et al. ) Videira, H. -D. ShinMANUSCRIPT & Crous, Sphaerulina chaenomelis (Y. Suto) Videira, U. Braun, H. -D. Shin & Crous, Sphaerulina koreana (Crous et al. ) Videira, H. -D. Shin & Crous; New names – Ramularia alangiicola Videira, H. -D. Shin & Crous, Ramularia veronicicola Videira & Crous; New species – Acrodontium fagicola Videira & Crous, Acrodontium luzulae Videira & Crous, Acrodontium pigmentosum Videira & Crous, Apseudocercosporella trigonotidis Videira, H. -D. Shin & Crous, Cercosporella catenulata Videira & Crous, Epicoleosporium ramularioides Videira, H. -D. Shin & Crous, Ramularia euonymicola Videira, H. -D. Shin, U. Braun & Crous, Ramularia gaultheriae Videira & Crous, Ramularia geraniicola Videira & Crous, Ramularia malicola Videira & Crous, Ramularia neodeusta Videira & Crous, Ramularia osterici Videira, H. -D. Shin & Crous, Ramularia rumicicola Videira, H. -D. Shin & Crous, Ramularia trigonotidis Videira, H. -D. Shin & Crous, Ramularia weberiana Videira & Crous, Ramulariopsis pseudoglycines Videira, Crous & Braun, Teratoramularia infinita Videira & Crous, Teratoramularia kirschneriana Videira & Crous, Teratoramularia persicariae Videira, H. -D. Shin & Crous, Teratoramularia rumicicola Videira, H. -D. Shin & Crous, Xenoramularia arxii Videira & Crous, Xenoramularia neerlandica Videira & Crous, Xenoramularia polygalicola Videira, H. -D. Shin & Crous; Typifications: Epitypifications – Cercosporella gossypii Speg., Cylindrosporium heraclei Oudem., Fusoma inaequale Preuss, Ovularia tovarae Sawada, Ramularia acroptili Bremer, Ramularia aplospora Speg., Ramularia armoraciae Fuckel, Ramularia beticola Fautrey & Lambotte, Ramularia geranii Fuckel, Ramularia lamii Fuckel var. lamii, Ramularia pusilla Unger, Ramularia vallisumbrosae Cavara, Ramularia variabilis Fuckel; Neotypifications ‒ Crocysporium rubellum Bonord., Ramularia collo- cygni B. Sutton & J.M. Waller; Lectotypification ‒ Ramularia kriegeriana Bres. Published online xxx; http://dx.doi.org/xxxxxx. Hard copy: xxx. INTRODUCTION Ramularia (Unger 1833)ACCEPTED is a species-rich genus (1 220 names listed in MycoBank, accessed 6 Nov. 2015) that belongs to the family Mycosphaerellaceae in the order Capnodiales . Ramularia species are mostly phytopathogenic and associated with leaf spots, necrosis or chlorosis, but some species can be saprobic or even mycophylic. The genus was monographed by Braun (1995, 1998) who defined Ramularia as genus of hyphomycetous species with hyaline conidiophores and conidia with distinct, thickened, darkened and refractive conidiogenous loci and conidial hila. Ramularia and allied genera were traditionally described based on the colour (hyaline or pigmented) and the structure of conidiophores (simple or branched), the structure of conidiogenous ACCEPTED MANUSCRIPT loci and conidial hila (conspicuous or inconspicuous, by being thickened and darkened or not). Genera with hyaline structures and conspicuous conidial loci include Cercosporella , Hawksworthiana , Neoovularia , Phacellium , Pseudodidymaria , Ramularia and Ramulariopsis , while genera with inconspicuous conidial loci include Monodidymaria , Neoramularia and Pseudocercosporella . Although these morphological characters have been considered important to define these genera, molecular studies have indicated that they are not always phylogenetically informative, and that the generic concepts need to be revised (Crous et al . 2001, Verkley et al. 2004, Kirschner 2009). The genus Cercosporella was usually distinguished from Ramularia by having bulging and hyaline conidiogenous loci. However, these characters are minute and difficult to observe with light microscopy, resulting in frequent transfers of species between both genera. Based on 28S nrDNA sequence data the type species of Cercosporella (C. virgaureae ) was shown to cluster in a sister clade to Ramularia s. str. (Kirschner 2009), and two additional characters were observed: Cercosporella has flat conidiogenous loci shaped as a truncated cone and produces cup-shaped appressoria. In contrast, Ramularia has conidiogenous loci with a raised rim with a tall central dome and a crater in between (resembling Cladosporium , see Bensch et al . 2012, 2015), and does not form appressoria. Species of Ramularia have Mycosphaerella sexual morphs, but only a few lifecycles have been experimentally proven, and some species may be asexual holomorphs (Braun 1995, 1998, Verkley et al . 2004, Videira et al. 2015b). Mycosphaerella s. lat. species have been associated with more than 30 genera, including both hyphomycetes and coelomycetes ( Mycosphaerellaceae ) (Crous 2009). Mycosphaerella s. str ., however, was shown to be confined to taxa with Ramularia asexual morphs (Verkley et al . 2004, Crous et al . 2009b, Videira et al . 2015b). In agreement with the new rules for naming of pleomorphic fungi in the International Code of Nomenclature for algae, fungi and plants (ICN; Hawksworth 2011, Hawksworth et al . 2011, Wingfield et al . 2012, Crous et al. 2015), the older name Ramularia was selected over that of Mycosphaerella (see Videira et al. 2015b for more details), and is included in a list of
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