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      Foliar pathogens of eucalypts

      research-article
      1 , 2 , , 2 , 3 , 4 , 5 , 6 , 2 , 7 , 8 , 9 , 10 , 11 , 1
      Studies in Mycology
      CBS Fungal Biodiversity Centre
      Corymbia, Eucalyptus, Foliar pathogen, New taxa, Taxonomy, Nowamycetaceae Crous, Lembosiniella Crous, Neosonderhenia Crous, Neothyriopsis Crous, Neotrichosphaeria Crous & Carnegie, Nothotrimmatostroma Crous, Nowamyces Crous, Walkaminomyces Crous & Carnegie, Disculoides fraxinoides Crous, Elsinoe piperitae Crous, Fusculina regnans Crous, Lembosiniella eucalyptorum Crous & Carnegie, Marthamyces johnstonii Crous & Carnegie, Neofusicoccum corticosae Crous & Summerell, Neosonderhenia eucalypti Crous, Neotrimmatostroma dalrympleanae Crous, Nowamyces globulus Crous, Nowamyces piperitae Crous, Phaeothyriolum dunnii Crous & Carnegie, Pseudophloeospora eucalyptigena Crous, Pseudophloeospora jollyi Crous, Quambalaria tasmaniae Crous, Quambalaria rugosae Crous, Sonderhenia radiata Crous, Teratosphaeria pseudonubilosa G. Pérez & Carnegie, Thyrinula dunnii Crous & Carnegie, Allelochaeta brevilata (H.J. Swart & D.A. Griffiths) Crous, Blastacervulus robbenensis (Crous et al.) Crous, Lembosiniella eucalypti (Sivan. & R.G. Shivas) Crous, Neofusicoccum versiforme (Z.Q. Yuan et al.) Crous, Neosonderhenia foliorum (Cooke) Crous, Neothyriopsis sphaerospora (Marasas) Crous, Neotrichosphaeria eucalypticola (Sivan. & R.G. Shivas) Crous & Carnegie, Nothotrimmatostroma bifarium (Gadgil & M.A. Dick) Crous, Nothotrimmatostroma eucalyptorum (Crous & Carnegie) Crous, Phacidium innumerum (Massee) Crous, Phaeothyriolum amygdalinum (Cooke & Massee) Crous & Carnegie, Phaeothyriolum corymbiae (Crous) Crous, Phaeothyriolum eucalyptorum (Crous & W.B. Kendr.) Crous, Pseudocercospora tumulosa (Carnegie & Beilharz) Carnegie & Crous, Teratosphaeria delegatensis (R.F. Park & Keane) Crous, Thyrinula parasitica (Crous) Crous, Walkaminomyces medusae (Carnegie & G.S. Pegg) Crous & Carnegie, Thyrinula uruguayensis Crous for Heteroconium eucalypti Crous & M.J. Wingf., Arnaudiella eucalyptorum Crous & W.B. Kendr., Lembosiopsis eucalyptina Petr. & Syd., Leptostromella eucalypti Cooke & Massee, Microthyrium amygdalinum Cooke & Massee, Mycosphaerella marksii Carnegie & Keane, Sphaerella cryptica Cooke, Stigmina robbenensis Crous et al., Thyriopsis sphaerospora Marasas, Trichosphaeria eucalypticola Sivan. & R.G. Shivas, Trimmatostroma bifarium Gadgil & M.A. Dick

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          Abstract

          Species of eucalypts are commonly cultivated for solid wood and pulp products. The expansion of commercially managed eucalypt plantations has chiefly been driven by their rapid growth and suitability for propagation across a very wide variety of sites and climatic conditions. Infection of foliar fungal pathogens of eucalypts is resulting in increasingly negative impacts on commercial forest industries globally. To assist in evaluating this threat, the present study provides a global perspective on foliar pathogens of eucalypts. We treat 110 different genera including species associated with foliar disease symptoms of these hosts. The vast majority of these fungi have been grown in axenic culture, and subjected to DNA sequence analysis, resolving their phylogeny. During the course of this study several new genera and species were encountered, and these are described. New genera include: Lembosiniella ( L. eucalyptorum on E. dunnii, Australia), Neosonderhenia ( N. eucalypti on E. costata, Australia), Neothyriopsis ( N. sphaerospora on E. camaldulensis, South Africa), Neotrichosphaeria ( N. eucalypticola on E. deglupta, Australia), Nothotrimmatostroma ( N. bifarium on E. dalrympleana, Australia), Nowamyces (incl. Nowamycetaceae fam. nov., N. globulus on E. globulus, Australia), and Walkaminomyces ( W. medusae on E. alba, Australia). New species include (all from Australia): Disculoides fraxinoides on E. fraxinoides, Elsinoe piperitae on E. piperita, Fusculina regnans on E. regnans, Marthamyces johnstonii on E. dunnii, Neofusicoccum corticosae on E. corticosa, Neotrimmatostroma dalrympleanae on E. dalrympleana, Nowamyces piperitae on E. piperita, Phaeothyriolum dunnii on E. dunnii, Pseudophloeospora eucalyptigena on E. obliqua, Pseudophloeospora jollyi on Eucalyptus sp., Quambalaria tasmaniae on Eucalyptus sp., Q. rugosae on E. rugosa, Sonderhenia radiata on E. radiata, Teratosphaeria pseudonubilosa on E. globulus and Thyrinula dunnii on E. dunnii. A new name is also proposed for Heteroconium eucalypti as Thyrinula uruguayensis on E. dunnii, Uruguay. Although many of these genera and species are commonly associated with disease problems, several appear to be opportunists developing on stressed or dying tissues. For the majority of these fungi, pathogenicity remains to be determined. This represents an important goal for forest pathologists and biologists in the future. Consequently, this study will promote renewed interest in foliar pathogens of eucalypts, leading to investigations that will provide an improved understanding of the biology of these fungi.

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          The Colletotrichum gloeosporioides species complex

          The limit of the Colletotrichum gloeosporioides species complex is defined genetically, based on a strongly supported clade within the Colletotrichum ITS gene tree. All taxa accepted within this clade are morphologically more or less typical of the broadly defined C. gloeosporioides, as it has been applied in the literature for the past 50 years. We accept 22 species plus one subspecies within the C. gloeosporioides complex. These include C. asianum, C. cordylinicola, C. fructicola, C. gloeosporioides, C. horii, C. kahawae subsp. kahawae, C. musae, C. nupharicola, C. psidii, C. siamense, C. theobromicola, C. tropicale, and C. xanthorrhoeae, along with the taxa described here as new, C. aenigma, C. aeschynomenes, C. alatae, C. alienum, C. aotearoa, C. clidemiae, C. kahawae subsp. ciggaro, C. salsolae, and C. ti, plus the nom. nov. C. queenslandicum (for C. gloeosporioides var. minus). All of the taxa are defined genetically on the basis of multi-gene phylogenies. Brief morphological descriptions are provided for species where no modern description is available. Many of the species are unable to be reliably distinguished using ITS, the official barcoding gene for fungi. Particularly problematic are a set of species genetically close to C. musae and another set of species genetically close to C. kahawae, referred to here as the Musae clade and the Kahawae clade, respectively. Each clade contains several species that are phylogenetically well supported in multi-gene analyses, but within the clades branch lengths are short because of the small number of phylogenetically informative characters, and in a few cases individual gene trees are incongruent. Some single genes or combinations of genes, such as glyceraldehyde-3-phosphate dehydrogenase and glutamine synthetase, can be used to reliably distinguish most taxa and will need to be developed as secondary barcodes for species level identification, which is important because many of these fungi are of biosecurity significance. In addition to the accepted species, notes are provided for names where a possible close relationship with C. gloeosporioides sensu lato has been suggested in the recent literature, along with all subspecific taxa and formae speciales within C. gloeosporioides and its putative teleomorph Glomerella cingulata. Taxonomic novelties: Name replacement - C. queenslandicum B. Weir & P.R. Johnst. New species - C. aenigma B. Weir & P.R. Johnst., C. aeschynomenes B. Weir & P.R. Johnst., C. alatae B. Weir & P.R. Johnst., C. alienum B. Weir & P.R. Johnst, C. aotearoa B. Weir & P.R. Johnst., C. clidemiae B. Weir & P.R. Johnst., C. salsolae B. Weir & P.R. Johnst., C. ti B. Weir & P.R. Johnst. New subspecies - C. kahawae subsp. ciggaro B. Weir & P.R. Johnst. Typification: Epitypification - C. queenslandicum B. Weir & P.R. Johnst.
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            The Colletotrichum acutatum species complex

            Colletotrichum acutatum is known as an important anthracnose pathogen of a wide range of host plants worldwide. Numerous studies have reported subgroups within the C. acutatum species complex. Multilocus molecular phylogenetic analysis (ITS, ACT, TUB2, CHS-1, GAPDH, HIS3) of 331 strains previously identified as C. acutatum and other related taxa, including strains from numerous hosts with wide geographic distributions, confirmed the molecular groups previously recognised and identified a series of novel taxa. Thirty-one species are accepted, of which 21 have not previously been recognised. Colletotrichum orchidophilum clusters basal to the C. acutatum species complex. There is a high phenotypic diversity within this complex, and some of the species appear to have preferences to specific hosts or geographical regions. Others appear to be plurivorous and are present in multiple regions. In this study, only C. salicis and C. rhombiforme formed sexual morphs in culture, although sexual morphs have been described from other taxa (especially as laboratory crosses), and there is evidence of hybridisation between different species. One species with similar morphology to C. acutatum but not belonging to this species complex was also described here as new, namely C. pseudoacutatum. Taxonomic novelties: New combinations - Colletotrichum limetticola (R.E. Clausen) Damm, P.F. Cannon & Crous, C. lupini (Bondar) Damm, P.F. Cannon & Crous, C. salicis (Fuckel) Damm, P.F. Cannon & Crous. New species - C. acerbum Damm, P.F. Cannon & Crous, C. australe Damm, P.F. Cannon & Crous, C. brisbanense Damm, P.F. Cannon & Crous, C. cosmi Damm, P.F. Cannon & Crous, C. costaricense Damm, P.F. Cannon & Crous, C. cuscutae Damm, P.F. Cannon & Crous, C. guajavae Damm, P.F. Cannon & Crous, C. indonesiense Damm, P.F. Cannon & Crous, C. johnstonii Damm, P.F. Cannon & Crous, C. kinghornii Damm, P.F. Cannon & Crous, C. laticiphilum Damm, P.F. Cannon & Crous, C. melonis Damm, P.F. Cannon & Crous, C. orchidophilum Damm, P.F. Cannon & Crous, C. paxtonii Damm, P.F. Cannon & Crous, C. pseudoacutatum Damm, P.F. Cannon & Crous C. pyricola Damm, P.F. Cannon & Crous, C. rhombiforme Damm, P.F. Cannon & Crous, C. scovillei Damm, P.F. Cannon & Crous, C. sloanei Damm, P.F. Cannon & Crous, C. tamarilloi Damm, P.F. Cannon & Crous, C. walleri Damm, P.F. Cannon & Crous. Typifications: Epitypifications - C. acutatum J.H. Simmonds, C. limetticola (R.E. Clausen) Damm, P.F. Cannon & Crous, C. nymphaeae (Pass.) Aa, C. phormii (Henn.) D.F. Farr & Rossman, C. salicis (Fuckel) Damm, P.F. Cannon & Crous. Lectotypifications - C. nymphaeae (Pass.) Aa, C. orchidearum Allesch.
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              The Botryosphaeriaceae: genera and species known from culture

              In this paper we give an account of the genera and species in the Botryosphaeriaceae. We consider morphological characters alone as inadequate to define genera or identify species, given the confusion it has repeatedly introduced in the past, their variation during development, and inevitable overlap as representation grows. Thus it seems likely that all of the older taxa linked to the Botryosphaeriaceae, and for which cultures or DNA sequence data are not available, cannot be linked to the species in this family that are known from culture. Such older taxa will have to be disregarded for future use unless they are epitypified. We therefore focus this paper on the 17 genera that can now be recognised phylogenetically, which concentrates on the species that are presently known from culture. Included is a historical overview of the family, the morphological features that define the genera and species and detailed descriptions of the 17 genera and 110 species. Keys to the genera and species are also provided. Phylogenetic relationships of the genera are given in a multi-locus tree based on combined SSU, ITS, LSU, EF1-α and β-tubulin sequences. The morphological descriptions are supplemented by phylogenetic trees (ITS alone or ITS + EF1-α) for the species in each genus. Taxonomic novelties: New species - Neofusicoccum batangarum Begoude, Jol. Roux & Slippers. New combinations - Botryosphaeria fabicerciana (S.F. Chen, D. Pavlic, M.J. Wingf. & X.D. Zhou) A.J.L. Phillips & A. Alves, Botryosphaeria ramosa (Pavlic, T.I. Burgess, M.J. Wingf.) A.J.L. Phillips & A. Alves, Cophinforma atrovirens (Mehl & Slippers) A. Alves & A.J.L. Phillips, Cophinforma mamane (D.E. Gardner) A.J.L. Phillips & A. Alves, Dothiorella pretoriensis (Jami, Gryzenh., Slippers & M.J. Wingf.) Abdollahz. & A.J.L. Phillips, Dothiorella thailandica (D.Q. Dai., J.K. Liu & K.D. Hyde) Abdollahz., A.J.L. Phillips & A. Alves, Dothiorella uruguayensis (C.A. Pérez, Blanchette, Slippers & M.J. Wingf.) Abdollahz. & A.J.L. Phillips, Lasiodiplodia lignicola (Ariyawansa, J.K. Liu & K.D. Hyde) A.J.L. Phillips, A. Alves & Abdollahz., Neoscytalidium hyalinum (C.K. Campb. & J.L. Mulder) A.J.L. Phillips, Groenewald & Crous, Sphaeropsis citrigena (A.J.L. Phillips, P.R. Johnst. & Pennycook) A.J.L. Phillips & A. Alves, Sphaeropsis eucalypticola (Doilom, J.K. Liu, & K.D. Hyde) A.J.L. Phillips, Sphaeropsis porosa (Van Niekerk & Crous) A.J.L. Phillips & A. Alves. Epitypification (basionym) - Sphaeria sapinea Fries. Neotypifications (basionyms) - Botryodiplodia theobromae Pat., Physalospora agaves Henn, Sphaeria atrovirens var. visci Alb. & Schwein.
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                Author and article information

                Contributors
                Journal
                Stud Mycol
                Stud. Mycol
                Studies in Mycology
                CBS Fungal Biodiversity Centre
                0166-0616
                1872-9797
                08 August 2019
                September 2019
                08 August 2019
                : 94
                : 125-298
                Affiliations
                [1 ]Westerdijk Fungal Biodiversity Institute, P.O. Box 85167, 3508 AD, Utrecht, The Netherlands
                [2 ]Department of Genetics, Biochemistry and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0002, South Africa
                [3 ]Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0002, South Africa
                [4 ]Department of Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai, 50200, Thailand
                [5 ]Forest Health & Biosecurity, Forest Science, NSW Department of Primary Industries – Forestry, Level 12, 10 Valentine Ave, Parramatta, NSW, 2150, Australia
                [6 ]School of Environment, Science and Engineering, Southern Cross University, Lismore, NSW, 2480, Australia
                [7 ]Environmental and Conservation Sciences, Murdoch University, 90 South Street, Murdoch, WA, 6150, Australia
                [8 ]Royal Botanic Gardens and Domain Trust, Mrs Macquaries Rd, Sydney, NSW, 2000, Australia
                [9 ]Agriculture Victoria Research, Department of Jobs, Precincts and Regions, AgriBio Centre, 5 Ring Road, LaTrobe University, Bundoora, Victoria, 3083, Australia
                [10 ]School of Applied Systems Biology, LaTrobe University, Bundoora, Victoria, 3083, Australia
                [11 ]Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, Australia
                Author notes
                [] Correspondence: P.W. Crous p.crous@ 123456wi.knaw.nl
                Article
                S0166-0616(19)30009-0
                10.1016/j.simyco.2019.08.001
                6797021
                31636729
                ec48febc-a02a-4431-aa66-fddf6ff66f9b
                © 2019 Westerdijk Fungal Biodiversity Institute. Production and hosting by ELSEVIER B.V.

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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                Research Paper

                Plant science & Botany
                corymbia,eucalyptus,foliar pathogen,new taxa,taxonomy,nowamycetaceae crous,lembosiniella crous,neosonderhenia crous,neothyriopsis crous,neotrichosphaeria crous & carnegie,nothotrimmatostroma crous,nowamyces crous,walkaminomyces crous & carnegie,disculoides fraxinoides crous,elsinoe piperitae crous,fusculina regnans crous,lembosiniella eucalyptorum crous & carnegie,marthamyces johnstonii crous & carnegie,neofusicoccum corticosae crous & summerell,neosonderhenia eucalypti crous,neotrimmatostroma dalrympleanae crous,nowamyces globulus crous,nowamyces piperitae crous,phaeothyriolum dunnii crous & carnegie,pseudophloeospora eucalyptigena crous,pseudophloeospora jollyi crous,quambalaria tasmaniae crous,quambalaria rugosae crous,sonderhenia radiata crous,teratosphaeria pseudonubilosa g. pérez & carnegie,thyrinula dunnii crous & carnegie,allelochaeta brevilata (h.j. swart & d.a. griffiths) crous,blastacervulus robbenensis (crous et al.) crous,lembosiniella eucalypti (sivan. & r.g. shivas) crous,neofusicoccum versiforme (z.q. yuan et al.) crous,neosonderhenia foliorum (cooke) crous,neothyriopsis sphaerospora (marasas) crous,neotrichosphaeria eucalypticola (sivan. & r.g. shivas) crous & carnegie,nothotrimmatostroma bifarium (gadgil & m.a. dick) crous,nothotrimmatostroma eucalyptorum (crous & carnegie) crous,phacidium innumerum (massee) crous,phaeothyriolum amygdalinum (cooke & massee) crous & carnegie,phaeothyriolum corymbiae (crous) crous,phaeothyriolum eucalyptorum (crous & w.b. kendr.) crous,pseudocercospora tumulosa (carnegie & beilharz) carnegie & crous,teratosphaeria delegatensis (r.f. park & keane) crous,thyrinula parasitica (crous) crous,walkaminomyces medusae (carnegie & g.s. pegg) crous & carnegie,thyrinula uruguayensis crous for heteroconium eucalypti crous & m.j. wingf.,arnaudiella eucalyptorum crous & w.b. kendr.,lembosiopsis eucalyptina petr. & syd.,leptostromella eucalypti cooke & massee,microthyrium amygdalinum cooke & massee,mycosphaerella marksii carnegie & keane,sphaerella cryptica cooke,stigmina robbenensis crous et al.,thyriopsis sphaerospora marasas,trichosphaeria eucalypticola sivan. & r.g. shivas,trimmatostroma bifarium gadgil & m.a. dick
                Plant science & Botany
                corymbia, eucalyptus, foliar pathogen, new taxa, taxonomy, nowamycetaceae crous, lembosiniella crous, neosonderhenia crous, neothyriopsis crous, neotrichosphaeria crous & carnegie, nothotrimmatostroma crous, nowamyces crous, walkaminomyces crous & carnegie, disculoides fraxinoides crous, elsinoe piperitae crous, fusculina regnans crous, lembosiniella eucalyptorum crous & carnegie, marthamyces johnstonii crous & carnegie, neofusicoccum corticosae crous & summerell, neosonderhenia eucalypti crous, neotrimmatostroma dalrympleanae crous, nowamyces globulus crous, nowamyces piperitae crous, phaeothyriolum dunnii crous & carnegie, pseudophloeospora eucalyptigena crous, pseudophloeospora jollyi crous, quambalaria tasmaniae crous, quambalaria rugosae crous, sonderhenia radiata crous, teratosphaeria pseudonubilosa g. pérez & carnegie, thyrinula dunnii crous & carnegie, allelochaeta brevilata (h.j. swart & d.a. griffiths) crous, blastacervulus robbenensis (crous et al.) crous, lembosiniella eucalypti (sivan. & r.g. shivas) crous, neofusicoccum versiforme (z.q. yuan et al.) crous, neosonderhenia foliorum (cooke) crous, neothyriopsis sphaerospora (marasas) crous, neotrichosphaeria eucalypticola (sivan. & r.g. shivas) crous & carnegie, nothotrimmatostroma bifarium (gadgil & m.a. dick) crous, nothotrimmatostroma eucalyptorum (crous & carnegie) crous, phacidium innumerum (massee) crous, phaeothyriolum amygdalinum (cooke & massee) crous & carnegie, phaeothyriolum corymbiae (crous) crous, phaeothyriolum eucalyptorum (crous & w.b. kendr.) crous, pseudocercospora tumulosa (carnegie & beilharz) carnegie & crous, teratosphaeria delegatensis (r.f. park & keane) crous, thyrinula parasitica (crous) crous, walkaminomyces medusae (carnegie & g.s. pegg) crous & carnegie, thyrinula uruguayensis crous for heteroconium eucalypti crous & m.j. wingf., arnaudiella eucalyptorum crous & w.b. kendr., lembosiopsis eucalyptina petr. & syd., leptostromella eucalypti cooke & massee, microthyrium amygdalinum cooke & massee, mycosphaerella marksii carnegie & keane, sphaerella cryptica cooke, stigmina robbenensis crous et al., thyriopsis sphaerospora marasas, trichosphaeria eucalypticola sivan. & r.g. shivas, trimmatostroma bifarium gadgil & m.a. dick

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