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The Type Species of Apiognomonia, A. Veneta, with Its Discula Anamorph Is Distinct from A

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The Type Species of Apiognomonia, A. Veneta, with Its Discula Anamorph Is Distinct from A mycological research 111 (2007) 693–709 journal homepage: www.elsevier.com/locate/mycres The type species of Apiognomonia, A. veneta, with its Discula anamorph is distinct from A. errabunda Mikhail V. SOGONOVa,b,*, Lisa A. CASTLEBURYb, Amy Y. ROSSMANb, James F. WHITEa aDepartment of Plant Biology & Pathology, Rutgers University, 59 Dudley Road, New Brunswick, New Jersey 08901-8520, USA bUSDA-ARS Systematic Botany & Mycology Laboratory, 10300 Baltimore Ave, Beltsville, Maryland 20705-2350, USA article info abstract Article history: Species of Apiognomonia with their Discula anamorphic states in the Gnomoniaceae, Diapor- Received 4 January 2006 thales, are known throughout the temperate Northern Hemisphere and cause diseases Received in revised form such as sycamore or plane tree anthracnose. The genus Apiognomonia was described based 26 February 2007 on A. veneta as the type species; however, there has been disagreement about whether or Published online 23 March 2007 not A. veneta is a synonym of A. errabunda. Using morphological, ecological, and DNA se- Corresponding Editor: quence data we conclude that A. errabunda and A. veneta are different species, although Brenda Wingfield very closely related; thus, A. veneta is the correct name for the type species of Apiognomonia. This conclusion is based on a combined analysis of sequences from the ITS regions of Keywords: nuclear rDNA for 51 isolates from host plants of eight genera and intron regions from actin, Anthracnose calmodulin and translation elongation factor 1-alpha for over 25 isolates. The type species Ascomycota of the genus Discula is D. nervisequa, the earliest available epithet for D. platani, the lectotype Diaporthales of Discula. D. nervisequa is the anamorph of A. veneta. Based on an examination of the type Endophytes specimen, we determined that the commonly used name for the anamorph of A. errabunda, Forest pathology D. umbrinella, refers to another species. A. veneta and A. errabunda including their ana- Gnomoniaceae morphs are described and illustrated. An account of all synonyms and excluded synonyms Nomenclature is presented. Species recognition Published by Elsevier Ltd on behalf of The British Mycological Society. Introduction diseases of Cornus (dogwood), Fagus (beech), Fraxinus (ash), Pla- tanus (sycamore, plane), and Quercus (oak) in North America Species of Apiognomonia with their Discula anamorphic states (Southworth 1889; Boewe et al. 1954; Neely & Himelick 1963, are known throughout the temperate Northern Hemisphere. 1965; Hepting 1971; Sinclair et al. 1987; Hibben & Daughtrey Like most members of the Gnomoniaceae as defined by Castle- 1988; Redlin 1991; Windham et al. 1994; Daughtrey et al. 1996; bury et al. (2002), species of Apiognomonia produce minute peri- Zhang & Blackwell 2001) and Europe (Sempio 1933a, 1933b; thecia on fallen, usually over-wintered, leaves. Conidial Butin & Zycha 1973; Sinclair et al. 1987; Morelet 1989; Fell structures are produced on living leaves and young twigs 1996; Tello et al. 2000). Plane tree anthracnose has also been while the inconspicuous teleomorph remains hidden in the reported from Australia (Milne & Hudson 1987), New Zealand leaf litter. A. errabunda and A. veneta, often reported as their (Brien 1939; Hitchcock & Cole 1978; Pennycook 1989), South Discula states, cause serious tree diseases such as anthracnose Africa (Swart et al. 1990), and South America (Sinclair et al. * Corresponding author. USDA-ARS, Systematic Botany & Mycology Laboratory, 10300 Baltimore Ave, Beltsville, Maryland 20705-2350, USA. E-mail address: [email protected] 0953-7562/$ – see front matter Published by Elsevier Ltd on behalf of The British Mycological Society. doi:10.1016/j.mycres.2007.03.013 694 M. V. Sogonov et al. 1987). A. errabunda, often as its Discula anamorph, is reported The main objective of this paper is to determine whether as one of the most common endophytes in healthy Fagus A. veneta and A. errabunda are separate species or synonyms. and Quercus trees (Sieber & Hugentobler 1987; Danti et al. 2002). Fresh isolates and herbarium specimens from a range of hosts The genus Apiognomonia is morphologically similar to Gno- were examined and characterized using DNA sequence data monia in the lack of stromata and having solitary perithecia and morphological features. A second objective is to deter- each with a central beak developing on leaves. Unlike Gnomo- mine the correct names for the species of Apiognomonia and nia having equally one-septate ascospores (Sogonov et al. the type species of Discula. The earliest name to be applied is 2005), Apiognomonia has been defined as having unequally based on an examination of authentic and type specimens two-celled ascospores (Mu¨ ller & von Arx 1962; Barr 1978, representing the numerous synonyms. Descriptions, illustra- 1991). In the original generic description, von Ho¨ hnel (1917) in- tions, and DNA sequences for all taxa are provided. troduced the genus Apiognomonia for leaf-inhabiting fungi that lack a stroma and produce upright, beaked perithecia with hy- aline, elongated to fusiform ascospores having two unequal Materials and methods cells. He stated that the ascospores were unequally one- septate without defining whether the upper or lower cell Preparation and morphological examination was larger. As a result Monod (1983) included species with of specimens and cultures a septum in either the upper or lower part of the ascospore, whereas Barr (1978) included only species with a septum in Fresh material was collected in Canada (British Columbia), the lower portion of the ascospore. Russia (Novgorod, Nizhniy Novgorod, Tver’ provinces), Historically, there has been confusion about the correct Switzerland (Geneve, Ticino, Vaud), and the USA (Maryland, names for the type and related species of both Apiognomonia Pennsylvania, Tennessee, Washington) in 2005–2006. Living and Discula. When von Ho¨ hnel (1917) established the genus and fallen leaves, and living, dead but still attached, and fallen Apiognomonia, he designated the type species as A. veneta twigs were examined for the presence of conidiomata and based on Laestadia veneta Sacc. & Speg. 1878, a fungus on Plata- ascomata. Those containing fungal structures were air-dried nus (Saccardo 1878), and did not mention any other species. In and stored in paper bags or envelopes. 1918, von Ho¨ hnel listed Apiognomonia with three additional Herbarium specimens were obtained from the US National species, A. errabunda (Rob.) Ho¨hn., A. erythrostoma (Fr.) Ho¨hn., Fungus Collections (BPI) as well as the Museum Botanicum and A. inaequalis (Auersw.) Ho¨ hn. Klebahn (1902) collected Berolinense (B), the Farlow Reference Library and Herbarium this species and sent it to Saccardo who considered Klebahn’s of Cryptogamic Botany in Harvard University (FH), the Royal collection to be L. veneta. However, Klebahn (1902) doubted the Botanic Garden at Kew (K), the Leiden University branch (L) placement of this fungus in Laestadia and renamed the fungus of the Nationaal Herbarium Nederland, the Muse´e et Jardins Gnomonia veneta (Sacc. & Speg.) Kleb. Later Klebahn (1914) Botanique Cantonaux in Lausanne (LAU), the Botanische found this binomial already in use for another species, Gnomo- Staatssammlung Mu¨ nchen (M), and the New York State nia veneta Speg. (Spegazzini 1879)onOstrya carpinifolia, and Museum Mycological Collections Herbarium (NYS). renamed the species based on L. veneta as G. platani Kleb. Fresh and herbarium material was first observed on natu- The earliest description of a fungus now referred to as ral substrata using a Wild M5A (Wild Heerbrugg, Heerbrugg, Apiognomonia errabunda (Roberge) Ho¨ hn. was by Roberge who Switzerland) or Leica MZ APO (Leica Microsystems, Weitzlar, observed a fungus on Fagus sylvatica and named it Sphaeria Germany) dissecting microscope and photographed with errabunda Roberge (in Desmazie`res 1848). Auerswald (1869) a DXM 1200 digital camera (Nikon Instruments, Melville, transferred this species to Gnomonia suggesting that it also NY). Perithecia and pycnidia-like conidiomata were extracted occurs on Quercus. After studying the biology of the fungi from leaf tissue with a sterile surgical scalpel under a dissect- from Quercus, Klebahn (1918) assigned the name Gnomonia ing microscope, placed into a drop of 3 % aqueous potassium quercina Kleb. stating that these fungi may also belong to the hydroxide, 7 % aqueous sodium acetate solution or water on species G. errabunda (Roberge) Auersw. on Fagus. Although a clean microscope slide. After rehydration, perithecia were some authors have recognized A. veneta based on Laestadia observed. Perithecia and pycnidia-like conidiomata were veneta to be the type species of Apiognomonia (Barr 1978), others crushed to release their contents, which were transferred have considered A. veneta to be a synonym of A. errabunda with an attenuated glass capillary or a scalpel to a clean (Boerema & Verhoeven 1972 as Gnomonia, Kobayashi 1970; area of the slide. For acervular conidiomata, a small part of Mu¨ ller & von Arx 1962; von Arx 1951). the conidial mass with some underlying hyphal mat inter- The anamorphic states of Apiognomonia have generally mixed with leaf tissue was extracted to a slide. Examined ma- been recognized in Discula Sacc. 1884 on twigs, and Gloeospo- terial was covered with a cover slip and observed under rium Desm. & Mont. 1856 on leaves. The link between these differential interference contrast (DIC) illumination with an two, as well as their links to the teleomorph,
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