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Pini, Causal Agents of Dothistroma Needle Blight of Pine

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Pini, Causal Agents of Dothistroma Needle Blight of Pine Received: 28 May 2016 | Accepted: 15 June 2016 DOI: 10.1111/efp.12304 REVIEW ARTICLE Neotypification of Dothistroma septosporum and epitypification of D. pini, causal agents of Dothistroma needle blight of pine I. Barnes1 | A. van der Nest1 | M. S. Mullett2 | P. W. Crous1,3 | R. Drenkhan4 | D. L. Musolin5 | M. J. Wingfield1 1Forestry and Agricultural Biotechnology Institute (FABI), Department of Summary Genetics, University of Pretoria, Pretoria, Dothistroma needle blight (DNB) is one of the most devastating needle diseases on South Africa Pinus spp. worldwide. Ever since the description of the causal agent of the disease in 2Forest Research, Alice Holt Lodge, Farnham, UK Europe in 1911 as Cytosporina septospora, and independently in the USA in 1941 as 3Centraalbureau voor Schimmelcultures Dothistroma pini, there has been considerable taxonomic discordance regarding the (CBS), Fungal Biodiversity Centre, Utrecht, name of the pathogen used in literature. This was compounded both by the proposal The Netherlands 4Institute of Forestry and Rural of different varieties of the pathogen based on differences in spore size and the appli- Engineering, Estonian University of Life cation of dual nomenclature where three names, Scirrhia pini, Eruptio pini and Sciences, Tartu, Estonia Mycosphaerella pini, were used to describe the sexual morph of the fungus. More 5Saint Petersburg State Forest Technical University, Saint Petersburg, Russia recent studies using sequence- based methods revealed that DNB can be caused by either one of two distinct species, that is D. septosporum and D. pini. These important Correspondence species have not been adequately typified, and this perpetuates lack of stability for Irene Barnes, Forestry and Agricultural Biotechnology Institute (FABI), Department their names. In this study, these names are fixed to reference sequences linked to liv- of Genetics, University of Pretoria, Pretoria, ing cultures representing type specimens. To achieve this goal, we designate an epi- 0002, South Africa. Email: [email protected] type for D. pini and a neotype for D. septosporum. The known polymorphism in the ITS region, the barcoding gene for these fungi, is characterized and a complete taxonomic Editor: S. Woodward history is provided for the genus Dothistroma. 1 | INTRODUCTION DNB can be caused by either one of two different fungal spe- cies, that is D. septosporum (Dorogin) M. Morelet and D. pini Hulbary Dothistroma needle blight (DNB), also commonly known as “red-band (Barnes, Crous, Wingfield, & Wingfield, 2004). These two species can disease,” “red spot” or “red- band needle blight,” is one of the most be clearly distinguished based on DNA sequence data (Barnes et al., important foliage diseases of Pinus spp. worldwide (Bradshaw, 2004; 2004; Ioos et al., 2010). However, before 2004, they were considered Drenkhan et al., 2016; Gibson, 1972). Symptoms of the disease include as one species and the names were commonly used interchangeably. reddish spots or bands surrounding black erumpent conidiomata This confusion in their taxonomy stems from two independent roots of (acervuli) on necrotic needles. Recent reviews of the disease distribu- the species name, one in Europe and the other in the USA (see Table 1). tion have shown that it occurs in 76 countries spanning a wide array In the USA, the asexual state of the pathogen was described by Robert of geographic and climatic conditions (Drenkhan et al., 2016; Woods L. Hulbary in 1941 as Dothistroma pini (Hulbary, 1941). The patho- et al., 2016). The disease occurs in almost all areas where suscepti- gen had also previously been described as Actinothyrium marginatum ble pines are found and has been documented on 95 Pinus species or (Saccardo, 1920), Cryptosporium acicola (Dearness, 1928), Septoria their subspecies. Rare and sporadic occurrences of the disease have acicola (Hedgcock, 1929) and it was confused with Lecanosticta aci­ also been recorded on five non- Pinus genera of the Pinaceae including cola (Sydow & Petrak, 1924), a closely related, but distinctly different Abies, Cedrus, Larix, Picea and Pseudotsuga. But in all these cases, heav- pathogen that causes brown- spot needle blight (Evans, 1984). ily diseased Pinus spp. have been in close proximity to those conifers In Europe, the pathogen causing DNB was first described as (Drenkhan et al., 2016). Cytosporina septospora (Doroguine, 1911). As was true in the USA, 388 | © 2016 Blackwell Verlag GmbH wileyonlinelibrary.com/journal/efp For. Path. 2016; 46: 388–407 B TABLE 1 Taxonomic history of Dothistroma species ARNES Date ET AL . material was Herbarium collection Confusion caused/importance/ Date Species epithet Reference Area Host (Pinus) collected details/number Description significance 1896 Hypostomum Vuillemin (1896) Theil- sur- Vanne, P. austriaca and April– No material deposited This is probably the first It is highly likely that this description is of flichianum Vuill. close to Sens P. mugo Turra Oct 1860 published description of either D. septosporum or D. pini in (Yonne), France subsp. P. mugo Dothistroma needle blight. The France. However, this cannot be (syn. P. mon­ work remained in obscurity validated as no herbarium material tana Mill.) until Morelet redescribed it as exists. Dothistroma flichianum in 1980. 1911 Cytosporina Doroguine (1911) In the park of the P. mugo Turra Summer Holotype material lost First recognized description of Doroguine described the symptoms as septospora Forestry subsp. P. mugo 1910 the Dothistroma pine needle “brownish–yellowish spots” or “darker Dorogin Institute in (syn. P. mon­ pathogen. brown spots” (Doroguine, 1912) causing Lesnoj, near to tana Mill.) this description to be overlooked in the St. Petersburg, literature. Later he transferred the name Russia to Brunchorstia pinea – see Doroguine, 1926. 1920 Actinothyrium Saccardo (1920) Orofino, Idaho, P. ponderosa 9 June 1917 IMI 91341; Shattuck Name given to fungus causing Erroneously described two fungi - see marginatum USA Laws Col. Weir No./Univ. red banding patterns on Sydow & Petrak (1924). Sacc. Padova No. 10330 P. ponderosa. 1924 Actinothyrium Sydow & Petrak Orofino, Idaho, P. ponderosa 9 June 1917 IMI 91341; Shattuck Realized that Saccardo had Called the fungus causing red band and marginatum = (1924) USA Laws Col. Weir No./Univ. described the fruiting body of brown spot the same thing, i.e. confused rejected as a Padova No. 10330 Leptostroma decipiens Petrak Lecanosticta acicola and Dothistroma spp. nomen confusum and the conidia of Lecanosticta This confusion was perpetuated by pini Thüm. From red- band Petrak (1961), Dearness (1928) as symptoms. Suggested that Cryptosporium acicolum Thüm., and A. marginatum therefore does Hedgcock (1929) as Septoria acicola not exist and proposed that (Thüm.) Sacc. See Siggers (1944). L. pini be synonymized with L. decipiens with the new name combination of Lecanosticta acicola (Thüm). Syd. 1926 Brunchorstia Doroguine (1926) As in 1911 and As in 1911 and As in 1911 No material deposited Doroguine mistakenly decided Called the red- band fungus Brunchorstia pinea (P. Karst.) various others various others and various that the fungus he described in pinea and this name was incorrectly Höhn others 1911 and 1912 as Cytosporina used to describe DNB in Eastern septospora was actually European literature – see Gremmen Brunchorstia pinea (another (1965) and Gremmen (1968). pathogen altogether). 1931 Septoriella Trotter (1931) Saccardo transferred Cytosporina Name change was never used in any septospora septospora to the genus further literature until 1968. (Dorogin) Sacc. Septoriella Oudem as S. apud Trotter septospora (Dorogin) Sacc. | (Continues) 389 390 TABLE 1 (Continued) | Date material was Herbarium collection Confusion caused/importance/ Date Species epithet Reference Area Host (Pinus) collected details/number Description significance 1941 Dothistroma pini Hulbary (1941) De Kalb County, P. nigra Arn. var. 29 Nov 1938 IILLS 27093; Described the red- band fungus. New genus = Dothistroma. Hulbary Illinois, USA austriaca MBT128093; herb A number of specimens from CBS H- 12211; IMI Ohio and Iowa considered 178710 conspecific with it. 1944 Actinothyrium Siggers (1944) Various states of Various Various Weir no. 10330; Examined a range of material Highlights the confusion often made in marginatum the USA 19906; 19930 (as from the USA and determined the literature between the brown- spot Sacc. = D. pini A. marginatum); F.P. that none of the various samples fungus and the red- band fungus. Clearly Hulbary 20548; F.P.41675 (as labelled as Actinothyrium stated that Lecanosticta acicola and Cryptosporium marginatum, Cryptosporium Dothistroma pini were different fungi. acicolum); F.P.18284 acicolum, Lecanosticta acicola and This work was later supported by (as Lecanosticta Septoria acicola were Murray & Batko (1962) when they acicola); F.P.54210; Lecanosticta acicola but were proposed the synonymy of Actinothyrium F.P.18237; F.P.46791 probably conspecific with D. pini marginatum and Dothistroma pini and (as Septoria acicola) as described by Hulbary. suggested retaining D. pini. Included in this was the original material used to describe Actinothyrium marginatum Sacc. (Weir no 10330). 1957 Mycosphaerella Munk (1957) Tvorup, Jutland, P. sylvestris 28 Oct 1880 IMI 287842 (slides) Sexual state described from Described the sexual stage of the (1880) pini Rostr. apud Denmark (possibly material collected by Emil pathogen but no link is made to any Munk P. maritima or Rostrup in 1880. asexual
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