ARTICLE 161 in in s. lat. (Saale), in vivo are in vivo, hyphomycetes taxonomy Key words: Ascomycota Cercospora names published in preparation for the inter alia and Passalora Passalora IMA FUNGUS · 7(1): 161–216 (2016) 161–216 · 7(1): FUNGUS IMA monograph, and meant to represent . 2012), including Art. 11 dealing Art. 11 et al. 2012), including . Cercospora detailed introduction, a survey of detailed introduction, (ICN; McNeill . To facilitate this process, careful examinations of all old To . ivecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get Any of the above conditions can be waived ivecommons.org/licenses/by-nc-nd/3.0/legalcode. ) 5. Species on dicots on dicots ) 5. Species in this fungal group whenever possible. On the other hand, in this fungal group whenever possible. exhibited symptoms and morphological characters still important in diagnosing plant pathogenic fungi, especially still important in diagnosing plant pathogenic purposes, but also for routine monitoring and identi cation the fungi concerned, in light of the ecology and taxonomy of Therefore, optimal which cause diseases on living plants. species should cover descriptions of new and already known the full range of traits ranging from characters limited number vitro to phylogenetic data. Currently only a and se uenced, of cercosporoid fungi has been cultivated from characters and hundreds of taxa are only known all names have to be taken into consideration vivo. However, to the rules of the for taxonomic purposes and are subject algae, fungi, and International Code of Nomenclature for plants Thus, all old names are applicable with the priority of names. when dealing with taxonomic-nomenclatural uestions, i.e. to nd correct names for certain taxa in accordance with the Code type collections and detailed descriptions are necessary and This is precisely the helpful for sound taxonomic conclusions. (1954) old, seriously sense of this series, based on Chupp’s outdated, an updated, supplementary treatment intended as a platform for the routine identi cation of cercosporoid fungi, including have spent decades modern molecular examinations. We examining thousands of old type collections and other samples of cercosporoid fungi, annotated list of Cercospora by Crous & Braun (2003). Numerous previously unpublished ). This fth contribution of this This fth contribution of this Ascomycota). ( Pseudocercospora rhoicola
et et et al. 3 et al. 2013, s. str. s. str.
sp. nov., and sp. nov., (Verkley (Verkley Cercospora et al. , which are described and illustrated in alphabetical order under the and illustrated in alphabetical order under the , which are described (Crous Ramularia ) includes Ascomycota) includes a younger heterotypic a younger heterotypic , Mycosphaeraella . 2013). The taxa The taxa et al. 2013). Mycosphaerellaceae Annonaceae , and Chiharu Nakashima , and Chiharu 2 ) to Annonaceae and s. lat.), belonging to Mycosphaerellaceae et al. 2009c, Wijayawardene
, which has been proposed as the , which has been proposed as the Capnodiales P. rhois-aromaticae rhois-aromaticae P. nom. nov., ( are often classi ed as ramularioid are often classi ed as ramularioid Mycosphaerella
et al. 2016, etc.). Cultures and molecular 2013, Bakhshi et al. 2014, Nguanhom , the eponymous genus, is associated , the eponymous genus, is associated Mycosphaerellaceae . 2015) and recommended for protection et al. 2015) and recommended for protection Cercospora Anacardiaceae et al. , Pedro W. Crous , Pedro W. et al. 2015). 1 The present paper is a continuation of a series of comprehensive taxonomic treatments of cercosporoid a continuation of a series of comprehensive The present paper is
you or your use of the work). work in the manner speci ed by the author or licensor (but not in any way that suggests that they endorse must attribute the You Ramularia P. guoana P. sp. nov., Cercosporoid fungi represent a very large group of CBS-KNAW, Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands Utrecht, 8, 3584 CT Fungal Biodiversity Centre, Uppsalalaan CBS-KNAW, Mie 514-8507, Japan Tsu, Kurima-machiya, 1577 Mie University, Graduate School of Bioresources, Martin-Luther-Universität, Institut für Biologie, Bereich Geobotanik und Botanischer Garten, Herbarium, Neuwerk 21, 06099 Halle und Botanischer Garten, Herbarium, Neuwerk Institut für Biologie, Bereich Geobotanik Martin-Luther-Universität, Germany; corresponding author e-mail: [email protected] Germany; corresponding 9 June 2016; Published: 16 June 2016. Accepted: Article info: Submitted: 1 February 2016; Abstract: fungi (formerly comprises species occurring on hosts belonging of cercosporoid fungi on dicots and series proceeds with treatments to the families © 2016 International Mycological Association © 2016 International Mycological conditions: distribute and transmit the work, under the following are free to share - to copy, You Attribution: Anacardiaceae (Anacardiaceae 2 3 1 Uwe Braun Cercosporoid fungi ( fungi Cercosporoid Non-commercial: No derivative works: For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creat transform, or build upon this work. may not alter, You purposes. may not use this work for commercial You permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. permission from the copyright holder. particular cercosporoid genera, supplemented by keys to the species concerned. A concerned. genera, supplemented by keys to the species particular cercosporoid key to the genera concerned, and a discussion of taxonomically relevant currently recognised cercosporoid genera, a The following taxonomic novelties are introduced: this series. characters were published in the rst part of cotini which are commonly referred to as cercosporoid fungi cercosporoid fungi which are commonly referred to as (Crous & Braun 2003, Braun holoblastic asexual concerned comprise dematiaceous, sexual morphs and at least partly mycosphaerella-like fungi within morphs. Corresponding mucedinaceous Mycosphaerellaceae fungi. with sexual morphs belonging to genera and species akin to the genus genera and species akin to the a phylogenetically The type species of the latter genus has proven asexual morph pertaining to One of the largest groups of fungi belonging to fungi belonging to One of the largest groups of Mycosphaerellaceae INTRODUCTION doi:10.5598/imafungus.2016.07.01.10 VOLUME 7 · NO. 1 preferred name (Crous al. 2004) making synonym of Ramularia 2014, Videira (Rossman 2015, Guatimosim se uence analyses should be used for taxonomic purposes plant pathogenic, leaf-spotting, economically relevant species causing diseases on a wide range of hosts, including numerous cultivated plants. In the last few decades, enormous taxonomic progress has been made by increasing application of molecular methods in capnodialean fungi, including Groenewald Braun et al.
results have been incorporated in already published issues morphological characters of the asexual morphs traditionally of the present series. Cultures, se uence analyses and used for the separation of genera do not re ect phylogenetic epitypi cations on the basis of cultured and se uenced entities (i.e. genera). A corresponding detailed phylogenetic collections represent the next phase in order to transfer the treatment of the Passalora complex is under preparation. All old morphology-based names into the era of consolidated results of modern studies dealing with cercosporoid fungi
ARTICLE species concepts. in Mycosphaerellaceae show that proper taxonomic results The growing number of DNA se uences of cercosporoid and conclusions have to be based on an integrated approach fungi allows better insights in the phylogenetic structure including molecular se uence analyses. Conclusions just of this fungal group on the familial as well as the generic based on morphological analyses are unreliable and do level. On the other hand, it has gradually been pointed not allow proper generic allocations. Therefore, we have out that traditionally applied phenotypic traits of the decided to revise the focus of the present series. Efforts to sexual as well as asexual morphs of cercosporoid fungi reassess and reallocate cercosporoid genera and species (Mycosphaerellaceae) are not in full agreement with will thus in future be based on re-examinations of types and genotypic generic circumscriptions. Species only forming other collections in combination with cultures and se uence mycosphaerella-like sexual morphs, i.e. without any asexual analyses whenever possible. The present series will not be fructi cations, are known in many currently recognised continued in its present form. In future, it will rather focus on cercosporoid genera (e.g. Guatimosim et al. 2016). As the revision of type collections of old cercosporoid species, a conse uence, the generic af nity of mycosphaerelloid including comprehensive descriptions and illustrations, ascomycetes cannot be properly resolved without cultures, which are necessary as basis for modern examinations in se uences, and phylogenetic analyses. On the other hand, vitro including subse uent se uence analyses. the classical morphological characters of asexual morphs So far four contributions have been published: part one of cercosporoid fungi are no longer reliable for allocating dealing with cercosporoid fungi on other fungi (mycophylic certain species to particular genera. The analysis of fern- taxa), on ferns as well as gymnosperms (Braun et al. 2013); inhabiting cercospoid fungi recently examined in Brazil part two dedicated to species on monocots, excluding true (Guatimosim et al. 2016) is a striking example. The genus grasses (Braun et al. 2014); part three with a treatment of Zasmidium is known to be polyphyletic (Crous et al. 2009a, cercosporoids on hosts of Poaceae (Braun et al. 2015a); b, Braun et al. 2013). Besides genuine species of Zasmidium and part four as the rst contribution to cercosporoids on s. str., zasmidium-like asexual morphs are also known for dicots covering species occurring on hosts belonging to the cercosporoid genera Neoceratosperma (Crous et al. the families Acanthaceae to Amaranthaceae (Braun et al. 2014, Guatimosim et al. 2016) and Paramycosphaerella 2015b). Part ve is a continuation covering cercosporoid (widened to include species with zasmidium-like asexual fungi on hosts of the dicot families Anacardiaceae and morphs by reallocations of Zasmidium aerohyalosporium, Z. Annonaceae. Generic descriptions and keys to accepted dicranopteridis, Z. nabiacense, and Mycosphaerella parkii genera are included in the rst part. The structure of the (i.e. Z. parkii; Guatimosim et al. 2016), i.e. cercosporoid present part follows the principles circumscribed in part 1 species with zasmidium-like morphology cannot be (Braun et al. 2013). properly assigned to cercosporoid genera without data from se uence analyses. The situation in all other cercosporoid genera is comparable. Pseudocercospora-like phenotypes MATERIALS AND METHODS of cercosporoid asexual morphs are usually connected with the genus Pseudocercospora s. str., but there are exceptions. The present work is a compilation based on our previous Several species morphologically not or barely distinguishable papers and unpublished data, as well as global literature. from true Pseudocercospora species do not cluster within Details of methods are given in the papers cited under the large Pseudocercospora clade and have been placed in References. As far as new examinations are concerned, Pallidocercospora and Phaeocercospora (Crous et al. 2012, fungal structures have been studied by standard methods 2013, Braun et al. 2013). Phaeophloeospora pteridivora is of light microscopy, using an Olympus BX50 microscope, an additional species with a pseudocercosporoid asexual with distilled water and lactic acid as mountants, but without morph that clusters in a clade with coelomycetous morphs any stain. If possible, measurements of 30 conidia and other (Guatimosim et al. 2016). The cercospora-like morphology structures have been made at a magni cation of ×1000. of conidiophores and conidia was believed to be a reliable All illustrations have been prepared by UB. The following character to assign species to Cercospora s. str., but even abbreviations are used: author names follow Brummit & in this genus there are exceptions, for example the recently Powell (1992), journals Bridson (2004a, b), and exsiccatae introduced genus Neocercospora (Bakhshi et al. 2015). http://www.botanischestaatssammlung.de/DatabaseClient/ However, the crux of the matter within Cercospora s. str. IndExs/index.jsp (IndExs – Index of Exsiccatae). Taxonomy is that reliable identi cations at species level are barely and nomenclature of plant families, genera and species possible without multigene analyses, above all within the are based on the “Angiosperm Phylogeny Website” (http:// Cercospora apii s. lat. complex (Groenewald et al. 2013). www.mobot.org/mobot/research/apweb/), Tropicos database Passalora s. lat. (sensu Crous & Braun 2003, Braun et al. (http://www.tropicos.org/), and The Plant List (http://www. 2013) is another strongly polyphyletic genus in which the theplantlist.org).
162 IMA FUNGUS Cercosporoid fungi 5
TAXONOMIC TREATMENT ARTICLE Cercosporoid species on dicots s. lat. (Anacardiaceae to Annonaceae)
Anacardiaceae
Cercospora
Key to Cercospora species on Anacardiaceae 1 External hyphae with solitary conidiophores present in vivo; conidia solitary or occasionally catenate, obclavate, base obconically truncate, to about 140 m long and 4–7.5 m wide; on Rhus semialata ...... see Passalora guoana Mycelium consistently internal in vivo; solitary conidiophores not developed; conidia consistently solitary, acicular, base truncate, 2–6 m wide ...... 2
2 (1) Leaf spots nally greyish brown to dingy greyish white with brown border; on Mangifera indica ...... C. mangiferae-indicae Leaf spots yellowish brown to blackish brown; on Rhus, Spondias, and Toxicodendron spp...... C. verniciferae
Tabular key to Cercospora species on Anacardiaceae according to host genera
Mangifera A single species ...... C. mangiferae-indicae
Rhus 1 External hyphae with solitary conidiophores present in vivo; conidia solitary or occasionally catenate, obclavate, base obconically truncate, to about 140 m long and 4–7.5 m wide ...... see Passalora guoana Mycelium consistently internal in vivo; solitary conidiophores not developed; conidia consistently solitary, acicular, base truncate, 2–5 m wide ...... Cercospora verniciferae
Spondias A single species ...... C. verniciferae
Toxicodendron A single species ...... C. verniciferae
Cercospora species on Anacardiaceae 2–20, erect, straight, subcylindrical or attenuated towards the tip, unbranched, not to moderately geniculate, 15–250 × 3–8 Cercospora mangiferae-indicae Munjal, Lall & m, pluriseptate, pale to medium brown or olivaceous brown Chona, Indian Phytopathol. 14: 185 (1962) [“1961”]. throughout or paler towards the tip, wall slighty thickened, (Fig. 1) smooth; conidiogenous cells integrated, terminal, sometimes intercalary, 15–40 m long, conidiogenous loci conspicuous, Literature: Crous & Braun (2003: 266), Kakoti et al. (1998), thickened and darkened, 2–4 m diam. Conidia solitary, Kamal (2010: 62), Todawat Nawalsing & Papdiwal (2011). acicular, straight to curved, 20–200 × 3–6 m, 1- to pluriseptate, hyaline, thin-walled, smooth, apex subacute, base truncate, Illustration: Munjal et al. (1962: 187, g. 6). 3–4.5 m wide, hila thickened and darkened.
Description: Leaf spots amphigenous, subcircular to irregular, Holotype: India: New Delhi, India Agricultural Research 1–25 mm diam, scattered to gregarious, pale to medium dark Institute, on Mangifera indica, 11 Dec. 1959, V. Prakash brown, later with greyish brown to dingy greyish white centre (HCIO 26847). and brown border on the upper leaf surface, brown with darker border below. Caespituli amphigenous, but mainly epiphyllous, Host range and distribution: On Mangifera indica, scattered, delicately punctiform, dark brown. Mycelium internal. Anacardiaceae, Asia (India, Asom, Delhi, Maharashtra, Tamil Stromata lacking or small, 10–30 m diam, substomatal or Nadu), West Indies (Dominican Republic). immersed, intraepidermal, only composed of a few swollen hyphal cells, 3–10 m diam, brown, wall somewhat thickened. Notes: This is a true Cercospora s. str., morphologically Conidiophores in small to moderately large fascicles, mostly belonging to C. apii s. lat., but with relatively broad conidia,
VOLUME 7 · NO. 1 163 Braun et al. ARTICLE
Fig. 1. Cercospora mangiferae-indicae (BPI 438068A). A. Fig. 2. Cercospora verniciferae (CUP 41508, lectotype). A. Conidiophore fascicle. B. Conidiophore tips. C. Conidia. Bar = 10 Conidiophore fascicle. B. Conidiophore tips. C. Conidia. Bar = 10 m. m.
3–6 m. Records from the Dominican Republic refer to Description: Leaf spots amphigenous, subcircular to angular- collections deposited as BPI 438068A,B. Conidiophores and irregular, 1.5–10 mm diam, later con uent and larger, conidia are morphologically barely distinguishable from those yellowish brown to blackish brown. Caespituli hypophyllous. of C. verniciferae. The phylogenetic af liation of this species Mycelium internal. Stromata absent or small, substomatal, is unknown. composed of a few dark brown cells. Conidiophores in small to moderately large fascicles, 2–20, arising from internal Cercospora verniciferae Chupp & Viégas, Bol. Soc. hyphae or stromatic hyphal aggregations, through stomata, Brasil. Agron. 8: 56 (1945). divergent, erect, straight, subcylindrical to somewhat (Fig. 2) geniculate, unbranched, 25–345 × 3–5.5 m, pluriseptate, medium to dark brown throughout or paler towards the tip, Literature: Chupp (1954: 44), Crous & Braun (2003: 420), wall thin to somewhat thickened, smooth; conidiogenous Guo et al. (2005: 32–33), Phengsintham et al. (2012: 50–51; cells integrated, terminal and intercalary, conidiogenous 2013: 98). loci conspicuous, 1.5–3 m diam. Conidia solitary, acicular, straight to curved or sinuous, 30–175 × 2–5 m, 3- to Illustration: Guo et al. (2005: 33, g. 14), Phengsintham et al. pluriseptate, hyaline, thin-walled, smooth, apex subacute, (2012: 52, g. 1a, 53, g. 1b; 2013: 99, gs 44–45). base truncate, 1.5–3 m wide, thickened and darkened.
164 IMA FUNGUS Cercosporoid fungi 5
Lectotype (designated here, MycoBank, MBT204884): Cercosporella toxicodendri (Ellis) U. Braun, Monogr. ARTICLE Brazil: São Paulo: Campinas, Santa Elisa Farm, Instituto Cercosporella, Ramularia and Allied Genera Agronomico, on Toxicodendron verniciferum [Rhus (Phytopath. Hyphom.) 2: 402 (1998). vernicifera], Anacardiaceae, 28 Apr. 1936, A. S. Costa 1518 Basionym: Cercospora toxicodendri Ellis, Amer. Naturalist (CUP 41508). Isolectotype: IACM 1518. 16: 811 (1882). Synonyms: Pseudocercospora toxicodendri (Ellis) X.J. Liu & Host range and distribution: On Rhus (chinensis var. Y.L. Guo, Mycosystema 2: 237 (1989). roxbourgii, succedanea), Spondias (dulcis, pinnata), Mycovellosiella toxicodendri (Ellis) U. Braun, Mycotaxon 55: Toxicodendron verniciferum, Anacardiaceae, Asia (Thailand), 224 (1995). Oceania (Samoa), South America (Brazil). Cercosporella californica Bonar, Mycologia 34: 188 (1942) [holotype: USA: California: San Mateo County, on Notes: This species belongs to the Cercospora apii Toxicodendron diversilobum, 15 Aug. 1935, L. Bonar s. lat. complex. The identity of morphologically barely (UC 653836); isotypes: BPI 420516, FH, MICH 15390, distinguishable collections on Spondias species from Asia WIS-F-11579]. and Oceania, referred to as C. verniciferae, is unclear and need molecular con rmation. The phylogenetic af liation of Literature: Saccardo (1886: 467), Chupp (1954: 43), Guo & C. verniciferae and its relation to C. mangiferae-indicae are Hsieh (1995: 14), Braun (1995a: 68; 1998: 402). unknown. Illustrations: Braun (1995: 69, g. 66, as C. californica). species Exsiccatae: Barthol., Fungi Columb. 4708. Ellis & Everh., Fungi Columb. 691. Ellis & Everh., N. Amer. Fungi 1524, Cercospora anacardii-occidentale Rangasw. et al., 1524b. &