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Reconsidering Species Boundaries in the Ceratocystis Paradoxa Complex, Including a New Species from Oil Palm and Cacao in Cameroon

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Reconsidering Species Boundaries in the Ceratocystis Paradoxa Complex, Including a New Species from Oil Palm and Cacao in Cameroon Mycologia, 106(4), 2014, pp. 757–784. DOI: 10.3852/13-298 # 2014 by The Mycological Society of America, Lawrence, KS 66044-8897 Reconsidering species boundaries in the Ceratocystis paradoxa complex, including a new species from oil palm and cacao in Cameroon Michael Mbenoun INTRODUCTION Z. Wilhelm de Beer Ceratocystis paradoxa is a soilborne fungal plant Michael J. Wingfield pathogen, widely distributed across the globe and Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute capable of infecting a broad range of hosts (Morgan- (FABI), Private Bag X20, University of Pretoria, Jones 1967, Anonymous 1987, Garofalo and McMillan Pretoria, 0028, South Africa 2004). First discovered associated with black rot of pineapple fruit in France by de Seynes (1886), the Brenda D. Wingfield impact of this fungus is best known from tropical, Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), Private Bag X20, subtropical and arid regions where it represents a University of Pretoria, Pretoria, 0028, South Africa serious constraint to the cultivation of monocotyle- donous crops (Kile 1993, Garofalo and McMillan 1 Jolanda Roux 2004). Some of the well known diseases caused by C. Department of Microbiology and Plant Pathology, paradoxa include rots of pineapple, sett rot of Forestry and Agricultural Biotechnology Institute (FABI), Private Bag X20, University of Pretoria, sugarcane and bud and trunk rots affecting almost Pretoria, 0028, South Africa all species of palm (Garafalo and McMillan 2004, Girard and Rott 2004). In most previous reports identification of C. Abstract: The Ceratocystis paradoxa complex accom- paradoxa was based on morphological characters of modates a group of fungal pathogens that have the fungus and relied primarily on two studies of become specialized to infect mostly monocotyledon- approximately 100 y ago. In the first of these, Petch ous plants. Four species currently are recognized in (1910) reviewed all earlier work and produced a this group, including C. paradoxa,whichhasa comprehensive account of the asexual state of the widespread distribution and broad host range. In this fungus. Dade (1928) subsequently described the study, multigene phylogenetic analyses involving sexual state and provided the first insights into the sequences of the ITS, b-tubulin and TEF-1a gene mating system of C. paradoxa. The power of DNA loci, in combination with phenotypic and mating sequencing technologies and molecular phyloge- studies, were used to characterize purported C. netics, which have deeply influenced fungal taxono- paradoxa isolates from Cameroon and to compare my during the past two decades, has not yet been fully them with isolates from elsewhere, including proto- explored in the recognition and delineation of C. logs and type specimens of known species. We show paradoxa and related species. that the C. paradoxa complex comprises substantially Ceratocystis belongs to the family Ceratocystidaceae, greater species diversity than previously recognized. order Microascales in the Sordariomycetes (Re´blova´ One new species in this group is described from et al. 2011, de Beer et al. 2013a) and is characterized Cameroon as Ceratocystis cerberus, while C. paradoxa by ascomata with bulbous bases and long necks that sensu stricto (s. str.) and four other species are give rise to ascospores in sticky masses (Hunt 1956, redefined. Lectotypes are designated for C. ethacetica Upadhyay 1981, Wingfield et al. 1993, Seifert et al. 2013). All species have tubular, phialidic conidio- and Endoconidium fragrans (synonym of C. ethace- phores with diverse forms of endoconidia. In addi- tica), while epitypes are designated for C. paradoxa tion, some species also produce thick-walled, pig- s. str., C. ethacetica and C. musarum. A neotype is mented conidia. Under the dual nomenclature designated for Catenularia echinata (synonym of C. system, the asexual states of Ceratocystis species were ethacetica) and two species, previously treated in treated in the genus Chalara (Nag Raj and Kendrick Thielaviopsis, are transferred to Ceratocystis. 1975) and were more recently consolidated in Key words: Ceratocystidaceae, Microascales, phy- Thielaviopsis (Paulin-Mahady et al. 2002). Based on logenetic species concept, Thielaviopsis DNA sequence analyses, it is now recognized that there are distinct phylogenetic lineages in Ceratocystis, defining complexes in which species have similar Submitted 13 Sep 2013; accepted for publication 7 Jan 2014. morphological and ecological characteristics (Har- 1 Corresponding author. [email protected] rington et al. 1996, Harrington and Wingfield 1998, 757 758 MYCOLOGIA Baker et al. 2003, Johnson et al. 2005, van Wyk et al. In addition to the two forms of endoconidia, species 2006). Indeed, it has been suggested that some of in the C. paradoxa complex also form what have been these lineages represent discrete genera (Wingfield referred to as chlamydospores or aleurioconidia. Went et al. 2013). The species related to C. paradoxa, (1893) described and illustrated pigmented conidia in sometimes referred to as C. paradoxa sensu lato (s. short chains on terminal ends of hyphae of Thiela- lat.), most likely represent one of these generic viopsis, while Peyronel (1918) established Chalaropsis entities within Ceratocystis. for species with aleuriospores borne solitarily at the Four species currently are recognized in the C. end of a branched conidiophore (Hennebert 1967). paradoxa complex, but results from phylogenetic These structures often have been called chlamydo- studies using sequences from single loci suggest that spores (Nag Raj and Kendrick 1975; Upadhyay 1981; this group includes at least two undescribed species van Wyk et al. 2007, 2009, 2011; Kamgan et al. 2008; (Harrington 2009, A´ lvarez et al. 2012). The previously Heath et al. 2009), but the term ‘‘aleurioconidia’’ was described species include C. paradoxa, C. radicicola reintroduced to taxonomic studies in Ceratocystis by (Bliss 1941), C. musarum (Riedl 1962) and Thiela- Paulin-Mahady et al. (2002). Seifert et al. (2011) use viopsis euricoi (Batista and Vital 1956, Paulin-Mahady the term aleurioconidia for ‘‘solitary, thallic conidia et al. 2002). The first two species are well known as that secede rhexolytically, usually with thickened and soilborne and pathogenic to monocotyledonous sometimes darkened walls’’ and distinguishes it from plants (Garofalo and McMillan 2004, Abdullah et al. chlamydospores, described as ‘‘thick-walled resting 2009). While C. paradoxa has been recognized as a spores, intercalary or terminal on hyphae … usually cosmopolitan fungus recorded on various hosts and not readily liberated’’. We concur with the definition from many parts of the world (Morgan-Jones 1967, of aleurioconidia by Paulin-Mahady et al. (2002) and Anonymous 1987), little is known regarding the Harrington (2009) as thick-walled, survival spores incidence of the other three species. For example, produced singly or in chains from the tips of there are no reports of C. musarum or T. euricoi other specialized hyphae, which also corresponds to the than from their first descriptions. definition by Seifert et al. (2011). The species in the C. paradoxa complex, of which The aim of this study is to characterize recent the sexual states are known, typically produce isolates resembling C. paradoxa s. lat. from oil palm characteristic digitate ornamentations on their asco- (Elaeis guineensis), cacao (Theobroma cacao)and matal bases (Dade 1928, Bliss 1941). Like many other pineapple (Ananas comosus) in Cameroon, with Ceratocystis species, the asexual states of these species multigene DNA phylogenies, morphology and mating often produce a variety of conidial forms in culture. tests. Species boundaries and previously suggested In his generic diagnosis of Thielaviopsis, Went (1893) synonymies of all species in the complex also are recognized two major types of conidia, endoconidia reconsidered. For this purpose, the Cameroonian (also referred to as phialoconidia, enteroblastic- isolates were compared with herbarium specimens phialidic ameroconidia), as opposed to thick-walled, and representative isolates of known species. pigmented conidia produced in chains at the tips of specialized hyphae. In most of the earlier studies the various forms of endoconidia were simply described MATERIALS AND METHODS as a range or continuum (as ‘‘cylindrical to ellipsoid/ Isolates.—Those forming the core material of this study doliiform, hyaline to brown’’; Bliss 1941, Hunt 1956, were collected in Cameroon in 2009 and 2010, during field Nag Raj and Kendrick 1975, Upadhyay 1981). surveys for Ceratocystis species occurring on pineapple, oil However, in the taxonomic literature of Ceratocystis palm and cacao. The surveys were conducted at various during the past decade, the endoconidia have been localities of the central, littoral and southwestern regions of described consistently as of two forms. These have the country. On cacao, fungi resembling C. paradoxa s. lat. been referred to as cylindrical versus doliform were isolated mostly from discarded pod husks (FIG. 1), but endoconidia (Baker-Engelbrecht and Harrington a few isolates also were obtained from artificially induced 2005, Johnson et al. 2005) or by other authors as wounds on the stems of cacao trees. Oil palm isolates were primary versus secondary conidia (van Wyk et al. obtained from trunks and stumps of felled trees, cut basal ends of leaf fronds and rotting palm-nut
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