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Fungal Systematics and Evolution PAGES 41–99 VOLUME 1 JUNE 2018 Fungal Systematics and Evolution PAGES 41–99 https://doi.org/10.3114/fuse.2018.01.04 Phylogeny and taxonomy of the genus Tubakia s. lat. U. Braun1*, C. Nakashima2, P.W. Crous3,4,5, J.Z. Groenewald3, O. Moreno-Rico6, S. Rooney-Latham7, C.L. Blomquist7, J. Haas8, J. Marmolejo9 1Martin-Luther-Universität, Institut für Biologie, Bereich Geobotanik und Botanischer Garten, Herbarium, Neuwerk 21, 06099 Halle (Saale), Germany 2Graduate School of Bioresources, Mie University, 1577 Kurima-machiya, Tsu, Mie 514–8507, Japan 3Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands 4Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands 5Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria 0028, South Africa 6Universidad Autónoma de Aguascalientes, Centro de Ciencias Básicas, Departamento de Microbiología, Av. Universidad No. 940, Colonia Cd. Universitaria, C. P. 20131 Aguascalientes, Ags., Mexico 7California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Plant Pest Diagnostics Lab, 3294 Meadowview Road, Sacramento, CA 95832-1448, USA 8US Forest Service, Stanislaus National Forest, 24545 Highway 120, Groveland, CA 95321, USA 9Laboratorio de Patología y Micología Forestal, Facultad de Ciencias Forestales, UANL, Carr. Nac. Km 145 Linares, N.L., Mexico *Corresponding author: [email protected] Key words: Abstract: The genus Tubakia is revised on the basis of morphological and phylogenetic data. The phylogenetic affinity Ascomycota of Tubakia to the family Melanconiellaceae (Diaporthales) was recently postulated, but new analyses based on sequences DNA phylogeny retrieved from material of the type species of Tubakia, T. dryina, support a family of its own, viz. Tubakiaceae fam. nov. epitypification Our phylogenetic analyses revealed the heterogeneity of Tubakia s. lat. which is divided into several genera, viz., Tubakia s. key str., Apiognomonioides gen. nov. (type species: Apiognomonioides supraseptata), Involutiscutellula gen. nov. (type species: Editor-in-Chief systematicsProf. dr P.W. Crous, Westerdijk Fungal Involutiscutellula Biodiversity Institute, P.O. rubra Box 85167, ), Oblongisporothyrium 3508 AD Utrecht, The Netherlands. gen. nov. (type species: Oblongisporothyrium castanopsidis), Paratubakia gen. E-mail: [email protected] Tubakiaceae nov. (type species: Paratubakia subglobosa), Racheliella gen. nov. (type species: Racheliella wingfieldianasp. nov.), Saprothyrium 24 new taxa gen. nov. (type species: Saprothyrium thailandense) and Sphaerosporithyrium gen. nov. (type species: Sphaerosporithyrium mexicanum sp. nov.). Greeneria saprophytica is phylogenetically closely allied to Racheliella wingfieldiana and is therefore reallocated to Racheliella. Particular emphasis is laid on a revision and phylogenetic analyses ofTubakia species described from Japan and North America. Almost all North American collections of this genus were previously referred to as T. dryina s. lat., which is, however, a heterogeneous complex. Several new North American species have recently been described. The new species Sphaerosporithyrium mexicanum, Tubakia melnikiana and T. sierrafriensis, causing leaf spots on several oak species found in the North-Central Mexican state Aguascalientes and the North-Eastern Mexican state Nuevo León, are described, illustrated, and compared with similar species. Several additional new species are introduced, including Tubakia californica based on Californian collections on various species of the generaChrysolepis , Notholithocarpus and Quercus, and T. dryinoides, T. oblongispora, T. paradryinoides, and Paratubakia subglobosoides described on the basis of Japanese collections. Tubakia suttoniana nom. nov., based on Dicarpella dryina, is a species closely allied to T. californica and currently only known from Europe. Tubakia dryina, type species of Tubakia, is epitypified, and the phylogenetic position and circumscription ofTubakia are clarified. A revised, supplemented key to the species of Tubakia and allied genera on the basis of conidiomata is provided. Published online: 1 March 2018. Dedicated to Vadim Alexandrovich Mel’nik (*16 March 1937, †10 April 2017). INTRODUCTION sheath of small fertile cells that give rise to one-celled, phialidic conidiogenous cells. The conidia are globose, subglobose, Tubakia species are endophytes in leaves and twigs of many ellipsoid, broad ellipsoid-obovoid to subcylindrical or somewhat tree species, but can also cause conspicuous leaf symptoms as irregular in shape, aseptate, hyaline, subhyaline to pigmented. plant pathogens (Cohen 1999, Gonthier et al. 2006, Hashizume The conidiomata and the conidia are distinct and readily allow et al. 2008, Sieber 2007). Obvious leaf spots are dotted with identification to generic level. Other fungal fruiting structures minute punctiform conidiomata (pycnothyria) composed of including crustose-pycnidial conidiomata on overwintering convex scutella with radiating threads of cells fixed to the twigs that open by lateral to irregular dehiscence or sporodochia substratum by a central columella, mostly surrounded by a formed on leaf veins (Holdenrieder & Kowalski 1989, Harrington Fungal Systematics and Evolution is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License © 2018 Westerdijk Fungal Biodiversity Institute 41 Braun et al. et al. 2012) may also be formed and have been described for species in North America is not well known, although it is likely T. dryina and T. iowensis. Some species produce a second type to contain more than just the single species listed in various of much smaller conidia (microconidia), either in “normal” publications asT . dryina. North American collections assigned to pycnothyria or in separate, mostly smaller pycnothyria. Reports T. dryina are undoubtedly heterogeneous, i.e., T. dryina in North of the occurrence and sporulation ofTubakia dryina as a saprobe America is a complex of cryptic species (Harrington et al. 2012). on necrotic tissue caused by other fungi (Munkvold & Neely An important contribution to resolve problems around the 1990) are unconfirmed and need further study and clarification. diversity of the T. dryina complex in North America has recently Tubakia was previously assigned to the Diaporthales within been published by Harrington & McNew (2018), including several Editor-in-Chief Prof. dr P.W. Crous, Westerdijk Fungal Biodiversity Institute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Ascomycota (Yokoyama & Tubaki 1971, Yun & Rossman 2011). In new species based on US collections. Several Tubakia samples a more detailed study on its phylogenetic affinity and position recently collected in Mexico on endemic oaks appear to be in the hierarchical system of the Ascomycota, Senanayake morphologically similar to T. dryina but are sufficiently distinct et al. (2017) placed Tubakia in the newly introduced family to suggest that they are undescribed species. A Tubakia causing Melanconiellaceae. The sexual morph of “T. dryina” has been serious oak diseases in California also appears to represent an referred to as Dicarpella dryina (Belisario 1991). However, D. additional undescribed species. Therefore, the present study dryina is not the type species of Dicarpella, and at least one presents a comprehensive examination and revision of Tubakia species, Dicarpella quercifolia was linked to Mastigosporella spp. in North America and worldwide, based on in vivo and in hyalina (≡ Harknessia hyalina; Barr 1979, Nag Raj & Di Cosmo vitro morphological analyses as well as phylogenetic data. This 1981, Rossman et al. 2015). Dicarpella quercifolia, together work has been accomplished in collaboration by an international with D. georgiana, were subsequently reallocated to the genus group of mycologists and phytopathologists from Asia, Europe Wuestneiopsis (Reid & Dawsett 1990). The relation and synonymy and North America. of Dicarpella and Tubakia are, however, unclear. Clarification requires phylogenetic data for D. bina, the type species of this genus, which is only known from the type collection. MATERIALS AND METHODS Saccardo (1913) introduced the genus Actinopelte for A. japonica, a scutellate fungus found in Japan on Castanea crenata Isolates (= C. pubinervis). Saccardo (l.c.) confused the large conidia of this species with asci, which was clarified and corrected by Theissen Isolates included in this study were obtained from symptomatic (1913: 509) who provided a detailed discussion, description, and leaves of diverse hosts, and identified as species of Tubakia illustration (Theissen 1913: 508, fig. VI) of A. japonica. Höhnel based on primarily the presence of pycnothyrial conidiomata (1925) revisited Actinopelte, added a new species, A. americana, and aseptate conidia. In addition, several isolates were obtained and introduced the new combination A. dryina, based on from the culture collection of the Westerdijk Fungal Biodiversity Leptothyrium dryinum. Yokoyama & Tubaki (1971) discussed the Institute (CBS culture collection), in Utrecht, The Netherlands, history of this genus in detail, published results of comprehensive the CDFA Plant Pathogen Collections (CDFA), Sacramento, USA, examinations of Japanese collections in vivo and in vitro, and and from the working
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