Fungal Diversity (2011) 51:43–61 DOI 10.1007/s13225-011-0146-5 Phyllosticta—an overview of current status of species recognition Saowanee Wikee & Dhanushka Udayanga & Pedro W. Crous & Ekachai Chukeatirote & Eric H. C. McKenzie & Ali H. Bahkali & DongQin Dai & Kevin D. Hyde Received: 17 October 2011 /Accepted: 18 October 2011 /Published online: 23 November 2011 # Kevin D. Hyde 2011 Abstract Phyllosticta is an important coelomycetous plant some novel taxa have been discovered. However, compared to pathogenic genus known to cause leaf spots and various the wide species diversity and taxonomic records, there is a fruit diseases worldwide on a large range of hosts. Species lack of molecular studies to resolve current names in the recognition in Phyllosticta has historically been based on genus. A phylogenetic tree is here generated by combined morphology, culture characters and host association. Al- gene analysis (ITS, partial actin and partial elongation factor though there have been several taxonomic revisions and 1α) using a selected set of taxa including type-derived enumerations of species, there is still considerable confu- sequences available in GenBank. Life modes, modal lifecycle sion when identifying taxa. Recent studies based on and applications of the genus in biocontrol and metabolite molecular data have resolved some cryptic species and production are also discussed. We present a selected set of taxa as an example of resolved and newly described species in the : : : : genus and these are annotated with host range, distribution, S. Wikee D. Udayanga E. Chukeatirote D. Dai K. D. Hyde disease symptoms and notes of additional information with Institute of Excellence in Fungal Research, comments where future work is needed. Mae Fah Luang University, Chiang Rai 57100, Thailand . : : : : Keywords Biocontrol Endophyte Guignardia Leaf S. Wikee D. Udayanga E. Chukeatirote D. Dai K. D. Hyde spot . Morphology. Molecular phylogeny. Secondary School of Science, Mae Fah Luang University, metabolites Chiang Rai 57100, Thailand P. W. Crous CBS−KNAW Fungal Biodiversity Centre, Introduction Uppsalalaan 8, 3584 CT Utrecht, The Netherlands The genus Phyllosticta Pers. ex Desm. is a taxonomically E. H. C. McKenzie confused group of microfungi comprising mostly important Landcare Research, phytopathogens with a wide host range (van der Aa 1973; Private Bag 92170, Auckland Mail Centre, van der Aa and Vanev 2002). Although the generic concept Auckland 1142, New Zealand of Phyllosticta has been refined and species names were D. Udayanga enumerated in a monographic treatment by van der Aa and State Key Laboratory of Mycology, Institute of Microbiology, Vanev (2002), species recognition still remains problematic Chinese Academy of Sciences, (Hyde et al. 2010a, b; Glienke et al. 2011). Several species No 3 1st West Beichen Road, Chaoyang District, Beijing 100101, People’s Republic of China of Phyllosticta have also been reported as endophytes and : saprobes (van der Aa and Vanev 2002; Baayen et al. 2002; A. H. Bahkali K. D. Hyde (*) Okane et al. 2003; Wulandari et al. 2009, 2010; Glienke et College of Science, Botany and Microbiology Department, al. 2011). Species of Phyllosticta (teleomorph Guignardia King Saud University, Riyadh, Saudi Arabia Viala & Ravaz) cause leaf spot symptoms and fruit diseases e-mail: [email protected] on a range of hosts including some economically important 44 Fungal Diversity (2011) 51:43–61 crops and ornamentals such as citrus, banana, apple, grapes, revision by van der Aa and Vanev (2002), a further nine cranberry, orchids, Ficus sp., Buxus sp. and maple (Uchida new species have been described (Box 1). and Aragaki 1980; Paul and Blackburn 1986; Baayen et al. 2002; McManus 1998; Olatinwo et al. 2003; Paul et al. Box 1 History of the study of Phyllosticta 2005; Liu et al. 2009). Phyllosticta species are also potential biocontrol agents (Yan et al. 2011), and have Year Event References been reported to produce novel bioactive metabolites such 1818 Phyllosticta was introduced Persoon (1818) as phyllostine and phyllostoxin (Evidente et al. 2008a). the generic name for Molecular data has improved the knowledge of species Sphaeria lichenoides DC. relationships and taxonomic classifications in the recent 1847 Phyllosticta Pers. was validated Desmazieres (1847) decade with reference to different complex groups of plant 1849 The genus Phyllosticta Pers. Kickx (1849) pathogenic fungi (Crous and Groenewald 2005; Shenoy et ex Desm typified with al. 2007; Rossman and Palm-Hernández 2008; Cai et al. Phyllosticta cruenta 2011; Udayanga et al. 2011). Similarly, Phyllosticta (and its (Kunze ex Fr.) Kickx (1849). sexual Guignardia state) is an important genus requiring 1968 Phyllosticta convallariae Pers. Donk (1968) designated as the type species modern revisionary treatment employing morphological 1927 A compilation of Phyllosticta Petrak and characters and a molecular phylogenetic approach, as the names published Sydow, (1927) understanding of species is less advanced, but molecular 1973 Phyllosticta outline with 46 Van der Aa data are expected to reveal cryptic novel species (Crous and accepted species (1973) Groenewald 2005; Hyde et al. 2010a, b). The objectives of 2002 A further revision of the species Van der Aa and this review are to (1) review the taxonomic and nomencla- described in Phyllosticta with Vanev (2002) tural history of Phyllosticta (2) review studies of species notes on each of the 191 accepted species recognition by morphological and molecular phylogenetic 2003-2011 P. ardisiicola Motohashi, I. Motohashi et al. criteria (3) discuss the life styles and biology of species of Araki & C. Nakash. (2008) the genus (4) summarize the applications of some species in P. aspidistricola Motohashi, metabolite production and biocontrol, and (5) provide notes I. Araki & C. Nakash. on selected resolved and recently described species. P. kerriae Motohashi, I. Araki & C. Nakash. P. fallopiae Motohashi, I. Araki & C. Nakash. History P. citriasiana Wulandari, Crous & Gruyter. The genus Phyllosticta Pers. was established by Persoon Phyllosticta (Guignardia) Wulandari et al. (1818) when he introduced the generic name Phyllosticta musicola N.F. Wulandari, L. (2009) for Sphaeria lichenoides DC. Over the past 200 years Cai & K. D. Hyde. Wulandari et al. numerous species have been added to the genus, often P. bifrenariae O.L. Pereira, (2010) C. Glienke & Crous. based on host association so that more than 3,100 names P. brazilianiae D. Stringari, Glienke et al. have been associated with Phyllosticta at various times C. Glienke & Crous. (2011) (http://www.indexfungorum.org/names/Names.asp: avail- P. citribraziliensis able 21 Sep, 2011). Desmazieres (1847) validated Phyllos- C. Glienke & Crous. ticta Pers., and Donk (1968) designated Phyllosticta Phyllosticta citrichinaensis H.X. Wang et al. 2011 convallariae Pers. as the type species. Many of the 3,100 Wang, K.D. Hyde & H.Y. Li names do not refer to what is now considered to be Phyllosticta sensu stricto. Initially, many fungi with The teleomorph state of Phyllosticta is Guignardia Viala unicellular conidia, similar to those of Phoma were named & Ravaz, represented by the generic type, Guignardia as either Phoma or Phyllosticta, depending on the location bidwellii (Ellis) Viala & Ravaz. There are 335 epithets of conidiomata on the host. Those fruiting on leaves were associated with this genus (http://www.indexfungorum.org/ described as Phyllosticta while those occurring on other names/Names.asp) and in a similar fashion to Phyllosticta, parts of the plant were placed in Phoma. van der Aa (1973) most species where described based on host association. provided a key for 46 species of Phyllosticta he accepted, The genus has not been well-studied, and there is no and this has been widely followed. Furthermore, in their comprehensive monograph, although individual species or monographic study, van der Aa and Vanev (2002) accepted groups of species have been treated (Hyde 1995; Motohashi 190 species in this genus, while Kirk et al. (2008) estimated et al. 2009; Wulandari et al. 2011). Most species of that there are only 92 Phyllosticta species. Since the Phyllosticta and Guignardia have been described indepen- Fungal Diversity (2011) 51:43–61 45 dently from each other, and only a few Phyllosticta species (2011). Because of this decision we use the name Phyllos- have been linked to their Guignardia teleomorphs. Conse- ticta throughout this review unless we specifically refer to a quently, their classification is confusing and the relation Guignardia species. Leptodothiorella, which previously between host range and disease are often poorly understood represented the spermatial state of some Phyllosticta species (van der Aa 2002) (e.g. Leptodothiorella aesculicola (Sacc.) Sivan.), are also treated as synonyms of Phyllosticta (van der Aa 1973). Using Phyllosticta versus Guignardia Morphological characteristics to differentiate species The name Phyllosticta (asexual state) and Guignardia (sexual state) have been used separately following the dual classifi- Phyllosticta pycnidia are usually globose, subglobose or cation system used by mycologists over several decades tympaniform, flattened above, and closely connected with the (Hawksworth 2004;McNeiletal.2006; Shenoy et al. 2007, subepidermal pseudostroma (Fig. 3a, b). They are mostly 2010). For instance Phyllosticta musarum (Cooke) Aa and unilocular but occasionally may be multilocular (van der Aa Guignardia musae Racib. are the same biological