Teratosphaeria Nubilosa, a Serious Leaf Disease Pathogen of Eucalyptus Spp

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Teratosphaeria Nubilosa, a Serious Leaf Disease Pathogen of Eucalyptus Spp MOLECULAR PLANT PATHOLOGY (2009) 10(1), 1–14 DOI: 10.1111/J.1364-3703.2008.00516.X PathogenBlackwell Publishing Ltd profile Teratosphaeria nubilosa, a serious leaf disease pathogen of Eucalyptus spp. in native and introduced areas GAVIN C. HUNTER1,2,*, PEDRO W. CROUS1,2, ANGUS J. CARNEGIE3 AND MICHAEL J. WINGFIELD2 1CBS Fungal Biodiversity Centre, PO Box 85167, 3508 AD, Utrecht, the Netherlands 2Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria 0002, Gauteng, South Africa 3Forest Resources Research, NSW Department of Primary Industries, PO Box 100, Beecroft 2119, NSW, Australia Useful websites: Mycobank, http://www.mycobank.org; SUMMARY Mycosphaerella identification website, http://www.cbs.knaw.nl/ Background: Teratosphaeria nubilosa is a serious leaf pathogen mycosphaerella/BioloMICS.aspx of several Eucalyptus spp. This review considers the taxonomic history, epidemiology, host associations and molecular biology of T. nubilosa. Taxonomy: Kingdom Fungi; Phylum Ascomycota; Class INTRODUCTION Dothideomycetes; Order Capnodiales; Family Teratosphaeriaceae; genus Teratosphaeria; species nubilosa. Many species of the ascomycete genera Mycosphaerella and Teratosphaeria infect leaves of Eucalyptus spp., where they cause Identification: Pseudothecia hypophyllous, less so amphig- a disease broadly referred to as Mycosphaerella leaf disease enous, ascomata black, globose becoming erumpent, asci apara- (MLD) (Burgess et al., 2007; Carnegie et al., 2007; Crous, 1998; physate, fasciculate, bitunicate, obovoid to ellipsoid, straight or Crous et al., 2004a, 2006b, 2007a,b). The predominant symptoms incurved, eight-spored, ascospores hyaline, non-guttulate, thin of MLD are leaf spots on the abaxial and/or adaxial leaf surfaces walled, straight to slightly curved, obovoid with obtuse ends, that vary in size, shape and colour (Crous, 1998). The leaf spots medially one-septate, slightly constricted at the median septum, often enlarge and coalesce to form larger blotches across the leaf tapering to both ends, ascospore germination type F, germinating surface, reducing the photosynthetic capability of trees, which from both ends, germ tubes growing parallel to the long axis of leads to premature leaf abscission (Park, 1988b; Pinkard and the spore with distortion of the primary ascospore cell. Mohammed, 2006). Premature defoliation reduces the growth of Host range: Teratosphaeria nubilosa is a primary pathogen susceptible Eucalyptus species, causing a decrease in the even- of several Eucalyptus spp., including E. botryoides, E. bicostata, tual wood volume of infected trees (Carnegie and Ades, 2003; E. bridgesiana, E. cypellocarpa, E. dunnii, E. globulus ssp. bicostata, Lundquist and Purnell, 1987; Milgate et al., 2005a). MLD there- E. globulus ssp. globulus, E. globulus ssp. maidenii, E. globulus fore poses a continued threat to the commercial propagation of ssp. pseudoglobulus, E. grandis, E. gunnii, E. nitens, E. pilularis, Eucalyptus species by forestry companies. E. quadrangulata, E. viminalis, E. grandis × E. resinifera and One of the most virulent species of Teratosphaeria causing dis- E. urophylla × E. globulus. ease on Eucalyptus is Teratosphaeria nubilosa (= Mycosphaerella Disease symptoms: Leaf spots predominantly occur on nubilosa). Since it was first identified in south-eastern Australia, juvenile Eucalyptus foliage; however, T. nubilosa has also T. nubilosa has been reported from several countries in Africa and recently been found on mature Eucalyptus foliage. Leaf spots are Europe, where it has become a major impediment to the continued amphigenous, varying in size from small spots that are round to propagation of cold-tolerant Eucalyptus spp. For example, the irregular. Lesions enlarge and coalesce to form larger blotches commercial propagation of E. globulus in South Africa was over the leaf surface. Initial lesions appear as pale-green spots abandoned in the 1930s because of its susceptibility to surrounded by purple margins and, once mature, are generally T. nubilosa (Lundquist and Purnell, 1987). Eucalyptus globulus yellow to pale brown with dark-brown raised borders. was later replaced with E. nitens in South Africa as a favoured cold-tolerant species grown at higher altitudes. Some provenances *Correspondence: E-mail: [email protected] of E. nitens, particularly those from Victoria, Australia, are also © 2008 BLACKWELL PUBLISHING LTD 1 2 G. C. HUNTER et al. susceptible to infection by T. nubilosa during the first 2–3 years et al. (2006b) to suggest that Mycosphaerella was not mono- of growth. Thus, the selection of planting stock resistant to this phyletic (Crous et al., 2001b; Goodwin et al., 2001). By employing disease has proven to be of paramount importance. nuclear large subunit sequence data for many Mycosphaerella Heavy outbreaks of MLD caused by T. nubilosa have also species from diverse hosts, Crous et al. (2007a) confirmed the occurred in Australia, including more than 95% defoliation of polyphyletic nature of Mycosphaerella, and revealed various species plantations of E. globulus in north-eastern New South Wales occurring on Eucalyptus to be more appropriately accommodated (Carnegie, 2007b). Teratosphaeria nubilosa was identified as the in Teratosphaeria. Thus, M. nubilosa was shown to be most main cause of severe damage and defoliation in an E. globulus appropriately accommodated in Teratosphaeria as T. nubilosa. plantation in Tasmania (Milgate et al., 2005a). In most instances, however, severe outbreaks of MLD in Australia are associated DISTRIBUTION OF T. NUBILOSA with T. nubilosa and T. cryptica occurring together (Barber et al., 2008; Carnegie et al., 1994; Carnegie and Ades, 2002; Park, Teratosphaeria nubilosa has been observed causing damage in 1988b). Eucalyptus globulus was replaced by E. nitens in north- plantations in most states of Australia, including Victoria (Barber western Tasmania as the preferred plantation species because of et al., 2008; Carnegie et al., 1994), Tasmania (Dungey et al., MLD (Mohammed et al., 2003). Severe defoliation (over 75%) 1997; Milgate et al., 2001), Western Australia (Jackson et al., has been observed in young E. globulus plantations in the 2008; Maxwell, 2004), New South Wales (Carnegie, 2007b) and Otways in Victoria in recent years. Previously only known from South Australia (Carnegie, 2000). Herbarium records confirmed juvenile and intermediate foliage (Crous, 1998; Park and Keane, by A. J. Carnegie reveal that T. nubilosa was identified in Queens- 1982a), T. nubilosa has recently been identified from adult land on E. globulus in the 1960s, but significant damage has not Eucalyptus foliage in eastern Australia (Kularatne et al., 2004; been reported. Teratosphaeria nubilosa has also been identified Maxwell et al., 2001), an aspect which could substantially from New Zealand (Dick, 1982; Dick and Gadgil, 1983), although increase the damage caused by this pathogen. T. cryptica is the most damaging species in this country (Dick, Considerable research has been conducted on T. nubilosa 1982; Dick and Gadgil, 1983; Hood et al., 2002), as the main during the course of the past 25 years. Most of the early research hosts planted are less susceptible to T. nubilosa. was focused on the taxonomy, host associations and the disease Several countries in Africa have identified T. nubilosa from caused by the pathogen. More recent studies have included commercial Eucalyptus plantations. Doidge (1950) first identified aspects related to the epidemiology, phylogeny, intraspecific T. nubilosa (as M. molleriana) from several Eucalyptus species in variation and population biology of this pathogen. The focus of South Africa. Currently, T. nubilosa is widespread within South this paper is to provide an overview of the literature pertaining Africa on various Eucalyptus species and can be found in several to T. nubilosa. Furthermore, we present opinions regarding the provinces, namely Gauteng, Kwa-Zulu Natal, Limpopo, Mpumalanga, status of knowledge and priorities for research on this increas- Eastern Cape and Western Cape (Crous, 1998; Crous et al., 2004a; ingly important pathogen. Crous and Wingfield, 1996; Hunter et al., 2004a,b; G. Perez, FABI, Pretoria, South Africa, unpublished data). Recent surveys in other African countries have also resulted in TAXONOMIC HISTORY the confirmation of T. nubilosa. Teratosphaeria nubilosa has been Sphaerella cryptica and S. nubilosa were originally described identified from south, south-western and western Ethiopia, from diseased Eucalyptus leaves collected near Melbourne, causing severe defoliation on E. globulus (Gezahgne et al., Australia (Cooke, 1891). These two ascomycetous fungi were to 2006). Eucalyptus plantations in Kenya, Tanzania and Zambia become two of the most well-recognized and important Eucalyptus have also been affected by T. nubilosa, where it has been leaf pathogens. Their placement in Sphaerella was incorrect and, identified causing defoliation of E. globulus (Crous et al., 2004a; after examination of the type material, S. cryptica and S. nubilosa Hunter et al., 2008). were transferred to Mycosphaerella (Hansford, 1956). Europe has also seen the introduction of T. nubilosa into its South Africa was one of the first countries to establish commercial Eucalyptus plantations. Collections of diseased Eucalyptus spp. in plantations for timber production. Initial E. globulus leaves from seven locations in Spain identified surveys of Eucalyptus in this country led Doidge (1950) to T. nubilosa causing leaf spots and premature
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