Species Concepts in Cercospora: Spotting the Weeds Among the Roses
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available online at www.studiesinmycology.org STUDIES IN MYCOLOGY 75: 115–170. Species concepts in Cercospora: spotting the weeds among the roses J.Z. Groenewald1*, C. Nakashima2, J. Nishikawa3, H.-D. Shin4, J.-H. Park4, A.N. Jama5, M. Groenewald1, U. Braun6, and P.W. Crous1, 7, 8 1CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands; 2Graduate School of Bioresources, Mie University, 1577 Kurima-machiya, Tsu, Mie 514–8507, Japan; 3Kakegawa Research Center, Sakata Seed Co., 1743-2 Yoshioka, Kakegawa, Shizuoka 436-0115, Japan; 4Division of Environmental Science and Ecological Engineering, College of Life Sciences and Biotechnology, Korea University, Seoul 136-701, Korea; 5Department of Agriculture, P.O. Box 326, University of Reading, Reading RG6 6AT, UK; 6Martin-Luther-Universität, Institut für Biologie, Bereich Geobotanik und Botanischer Garten, Herbarium, Neuwerk 21, 06099 Halle (Saale), Germany; 7Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands; 8Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands *Correspondence: Johannes Z. Groenewald, [email protected] Abstract: The genus Cercospora contains numerous important plant pathogenic fungi from a diverse range of hosts. Most species of Cercospora are known only from their morphological characters in vivo. Although the genus contains more than 5 000 names, very few cultures and associated DNA sequence data are available. In this study, 360 Cercospora isolates, obtained from 161 host species, 49 host families and 39 countries, were used to compile a molecular phylogeny. Partial sequences were derived from the internal transcribed spacer regions and intervening 5.8S nrRNA, actin, calmodulin, histone H3 and translation elongation factor 1-alpha genes. The resulting phylogenetic clades were evaluated for application of existing species names and five novel species are introduced. Eleven species are epi-, lecto- or neotypified in this study. Although existing species names were available for several clades, it was not always possible to apply North American or European names to African or Asian strains and vice versa. Some species were found to be limited to a specific host genus, whereas others were isolated from a wide host range. No single locus was found to be the ideal DNA barcode gene for the genus, and species identification needs to be based on a combination of gene loci and morphological characters. Additional primers were developed to supplement those previously published for amplification of the loci used in this study. Key words: Cercospora apii complex, co-evolution, host jumping, host specificity, speciation. Taxonomic novelties: New species - Cercospora coniogrammes Crous & R.G. Shivas, Cercospora delaireae C. Nakash., Crous, U. Braun & H.D. Shin, Cercospora euphorbiae-sieboldianae C. Nakash., Crous, U. Braun & H.D. Shin, Cercospora pileicola C. Nakash., Crous, U. Braun & H.D. Shin, Cercospora vignigena C. Nakash., Crous, U. Braun & H.D. Shin. Typifications: epitypifications - Cercospora alchemillicola U. Braun & C.F. Hill, Cercospora althaeina Sacc., Cercospora armoraciae Sacc., Cercospora corchori Sawada, Cercospora mercurialis Pass., Cercospora olivascens Sacc., Cercospora violae Sacc.; neotypifications - Cercospora fagopyri N. Nakata & S. Takim., Cercospora sojina Hara. Published online: 26 September 2012; doi:10.3114/sim0012. Hard copy: June 2013. INTRODUCTION fruits and seeds or were associated with postharvest fruit rot disease (Silva & Pereira 2008) of hosts from across the world (Agrios 2005, Species of the genus Cercospora belong to one of the largest genera To-Anun et al. 2011). The cercosporoid fungi have also been used as of hyphomycetes and were often linked to the teleomorph genus biocontrol agents (Morris & Crous 1994, Inglis et al. 2001, Tessman Mycosphaerella (Capnodiales, Mycosphaerellaceae; Stewart et al. et al. 2001). Species of Cercospora were traditionally named after the 1999, Crous et al. 2000). The genus Mycosphaerella was shown host from which they were isolated, even to the extent that a species to be polyphyletic (Crous et al. 2007), and subsequently split into of Cercospora was described as new when found on a different numerous genera, correlating with its different anamorph states host plant (Chupp 1954, Ellis 1971). The genus Cercospora was (Crous et al. 2009a, b). The genus Cercospora is now considered first erected by Fresenius for passalora-like fungi with pluriseptate a holomorphic genus in its own right, with some species exhibiting conidia (in Fuckel 1863). Chupp’s (1954) monograph accepted 1 419 the ability to form mycosphaerella-like teleomorphs (Corlett 1991, Cercospora species and proposed a broad concept for this genus Crous et al. 2004b). Mycosphaerella s. str. on the other hand, is based on whether hila were thickened or not, and whether conidia restricted to taxa that form Ramularia anamorphs (Verkley et al. were pigmented, single or in chains. The number of Cercospora 2004). As Mycosphaerella has been widely applied to more than 40 species doubled to more than 3 000 when Pollack (1987) published different genera, Crous et al. (2009b) expressed their preference her annotated list of Cercospora names. Since then a combination of to use the older, recently monographed (Braun 1998) anamorph- characters such as conidiomatal structure, mycelium, conidiophores, typified nameRamularia (1833) for this holomorphic clade, instead conidiogenous cells and conidia has been used to divide the genus of the younger, confused teleomorph-typified generic name into morphologically similar units. Crous & Braun (2003) used the Mycosphaerella (1884). This is allowed under the new, changed structure of conidiogenous loci and hila as well as the absence or Article 59 of the International Code for Nomenclature of algae, presence of pigmentation in conidiophores and conidia in their fungi, and plants (ICN) (Hawksworth 2011, Norvell 2011). revision of names published in Cercospora and Passalora. They Species of Cercospora are commonly associated with leaf spots recognised 659 names in the genus Cercospora, with a further 281 (Fig. 1), and have also been isolated from necrotic lesions of flowers, names referred to as C. apii s. lat. The C. apii complex represented Copyright CBS-KNAW Fungal Biodiversity Centre. Open access under CC BY-NC-ND license. You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. Studies in Mycology For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 115 GROENEWALD ET AL. Fig. 1. Foliar disease symptoms associated with Cercospora spp. A. C. achyranthis on Achyranthes japonica. B. C. dispori on Disporum viridescens. C. C. chinensis on Polygonatum humile. D. C. cf. flagellaris on Amaranthus patulus. E. C. capsici on Capsicum annuum. F. Cercospora sp. on Ajuga multiflora. G. Cercospora sp. on Cardamine leucanthe. H. C. cf. flagellaris on Celosia argentea var. cristata. I. C. zeina on Zea mays. J. C. beticola on Beta vulgaris. K. C. chrysanthemi on Chrysanthemum. L. C. apii on Apium. M. C. amoraciae on Rorippa indica. N. C. beticola on Chrysanthemum segetum. O. C. apiicola on Apium. P. C. ipomoeae on Persicaria thunbergii. Q. C. althaeina on Althaea rosea. R. C. zebrina on Trifolium repens. S. C. sojina on Glycine max. T. C. brunkii on Geranium nepalense. 116 SPECIEs CONCEPTs IN CERcOSPORA Cercospora species that were morphologically indistinguishable species (Groenewald et al. 2010a). For example, Goodwin et al. from C. apii (Ellis 1971, Crous & Braun 2003). In addition, Crous & (2001) found a mean of 1.27 sequence changes over 18 taxa Braun (2003) introduced the concept of “compound species” which from 11 Cercospora species, and Pretorius et al. (2003) found a consisted of morphologically indistinguishable species with different mean of 1.64 changes when they tested 25 taxa representing 11 races (host range), genetically uniform or heterogeneous, with Cercospora species. Both Goodwin et al. (2001) and Pretorius different degrees of biological specialisation. They also proposed that et al. (2003) observed more transitions than transversions. Only genetically and morphologically clearly distinguishable taxa should a limited number of studies utilising gene sequences other than be treated as separate species, although the study was confounded ITS have been published thus far (for example Tessmann et al. by the general unavailability of Cercospora cultures for DNA 2001, Crous et al. 2004b, Groenewald et al. 2005, 2006a, 2010a, analyses. Ex-type strains mostly do not exist as such isolates were Montenegro-Calderón et al. 2011). Tessmann et al. (2001) found neither designated nor preserved, for the majority of Cercospora that 14 of the 431 aligned translation elongation factor 1-alpha species (Groenewald et al. 2010a).