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Neonectria and Cylindrocarpon: the Nectria Mammoidea Group and Species Lacking Microconidia

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Neonectria and Cylindrocarpon: the Nectria Mammoidea Group and Species Lacking Microconidia Mycologia, 96(3), 2004, pp. 572±597. q 2004 by The Mycological Society of America, Lawrence, KS 66044-8897 Neonectria and Cylindrocarpon: the Nectria mammoidea group and species lacking microconidia David Brayford anamorphs. A key to nectriaceous species of Neonec- International Mycological Institute, Bakeham Lane, tria that have Cylindrocarpon anamorphs that lack mi- Egham, Surrey, England TW20 9TY croconidia and chlamydospores and/or that have a Barry M. Honda N. mammoidea type perithecial wall anatomy is pre- Department of Molecular Biology and Biochemistry, sented. New combinations are proposed for other Simon Fraser University, Burnaby, British Columbia, species formerly included in Nectria that have non- V5A 1S6 Canada microconidial Cylindrocarpon anamorphs: Neonectria cinnamomea, Neo. jungneri, Neo. platycephala, Neo. Feky R. Mantiri phaeodisca and Neo. verrucospora. Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia, Key words: forest pathology, Hypocreales, mito- V5A 1S6 Canada chondrial rDNA, Nectria, Nectriaceae, phylogeny, sys- tematics Gary J. Samuels1 United States Department of Agriculture, Agriculture Research Service, Systematic Botany and Mycology INTRODUCTION Laboratory, Room 304, B-011A, 10300 Baltimore Ave., Beltsville, Maryland 20705-2350 The genus Nectria Fr. (Hypocreales: Nectriaceae) is a classic genus of pyrenomycetes in the sense that its species have been known since it was described early Abstract: Neonectria (Hypocreales: Nectriaceae) spe- in the 19th century, and over the years many species cies having Cylindrocarpon anamorphs that lack mi- from temperate and tropical regions have been in- croconidia and chlamydospores include: Neo. disco- cluded in it. The stereotypical nectria has a brightly phora var. discophora, Neo. discophora var. rubi, stat colored peritheciumÐusually redÐthat is seated di- nov. et comb. nov., Neo. lucida, comb. nov., Neo. vir- rectly on a woody substratum (e.g., Booth 1959). idispora, sp. nov. and Neo. westlandica, comb. nov. Closer consideration of the diversity that has been Perithecia of these species are red and perithecial included in Nectria, along with DNA sequence anal- anatomy is of the N. mammoidea type, with a pali- ysis has shown the genus to be polyphyletic. Nectria sade of hypha-like cells in the outer perithecial wall. now is restricted to its type, N. cinnabarina (Tode : These species occur on recently dead or dying trees. Fr.) Fr., and a relatively small number of similar spe- Perithecia of Neo. betulae, sp. nov and Neo. dumontii, cies (Rossman 1989, Rehner and Samuels 1994, Ross- sp. nov. are anatomically and biologically similar to man et al 1999). Many species of Nectria sensu lato those of Neo. discophora. The only known culture of have been placed in other genera and families (Ross- Neo. betulae remained sterile, while Neo. dumontii has man et al 1999, 2001, Schroers 2002). Rossman et al not been cultured; their anamorphs are presumed to (1999) and Mantiri et al (2001) resurrected Neonec- be Cylindrocarpon. Analyses of mit ssu rDNA sequenc- tria Wollenw. for former Nectria species that have Cy- es indicate that Neonectria/Cylindrocarpon is mono- lindrocarpon Wollenw. anamorphs. The only known phyletic. Within the genus, species having N. mam- teleomorphs of Cylindrocarpon are Neonectria. Mantiri moidea type perithecia are paraphyletic. Most species et al (2001) used mitochondrial small-subunit ribo- cluster with Neo. discophora, but Neo. westlandica and somal (mit ssu rDNA) sequences with a selected Neo. trachosa are basal to a clade that includes species group of species to show that Cylindrocarpon, and that do not have a N. mammoidea-type perithecium. therefore Neonectria, is monophyletic. Nectria fuckeliana clusters independently of Neonec- In the present paper we continue describing or re- tria and Nectria. Although reported to have a Cylin- describing species of Nectria s. lat. that have Cylindro- drocarpon anamorph, fresh ascospore isolates of N. fuckeliana did not produce Cylindrocarpon macroco- carpon anamorphs (Brayford and Samuels 1993, Sa- nidia but produced acremonium- or verticillium-like muels and Brayford 1990, 1993, 1994). We discuss species of Neonectria that have been or could have Accepted for publication October 10, 2003. been placed in the Nectria mammoidea group of Nec- 1 Corresponding author. E-mail: [email protected] tria (Booth 1966) because of their perithecial wall 572 BRAYFORD ET AL: NEONECTRIA AND CYLINDROCARPON 573 anatomy. Throughout this paper, these abbreviations surface layers of pseudoparenchymatous cells over are used: N. 5 Nectria, Neo. 5 Neonectria. the N. mammoidea palisade. Perithecia of species of Neonectria that have an N. Ascospores in the N. mammoidea Group are typi- mammoidea wall structure often arise from a char- cally ellipsoidal and hyaline, becoming pale brown at acteristic stroma, here termed the N. mammoidea- maturity; they are usually 1-septate, but those of N. type stroma. In this stromal type, compacted hyphae phaeodisca Rossman are phragmosporous (Rossman grow within cells of the cortex. Densely packed, dis- 1983, Samuels and Brayford 1993). The ascospores crete hyphae, ca 3.5 mm wide, arise from these stro- usually are smooth but often are spinulose. Typically mal cells and extend perpendicular to the substra- the developing ascospores are surrounded by a thin , m tum, surrounding the perithecial base (see FIG. 51). ( 1 m) sheath, contraction of which may result in Such a stroma is seen rarely in species that do not the ornamentation. Ascospores with a distinctly wart- have a N. mammoidea wall, such as Nectria vermispora ed, tuberculate or striate ornamentated sheath such Samuels & Brayford (Samuels and Brayford 1993) as found in the Neo. veuillotiana (Sacc. & Roum.) and N. hypoxantha Penz. & Sacc. (Samuels 1976), nei- Brayford & Samuels Group (Brayford and Samuels ther of which has been linked to any anamorph. 1993) have not been observed in taxa of the N. mam- The Cylindrocarpon anamorphs of these fungi lack moidea Group. Discharged ascospores are typically microconidia and chlamydospores and for these rea- pale yellow-brown and are usually spinulose. The re- mains of apical paraphyses are usually not conspicu- sons were included in Cylindrocarpon ``Group 2'' by ous among mature asci. Booth (1966). All species included in this group were The Cylindrocarpon anamorphs of Group 2 (the N. anamorphs of members of the ``Nectria mammoidea mammoidea Group) form round-ended, slightly ar- Group''. Following Booth (1959, 1966) this group is cuate macroconidia but lack microconidia and chla- centered on N. mammoidea Phill. & Plowr., a later mydospores (Booth 1959, 1966). However, we have taxonomic synonym of N. discophora (Mont.) Mont. found some exceptions to this generalization. Neo- (5 Neo. discophora [Mont.] Mantiri & Samuels). In nectria betulae has a typically N. mammoidea perithe- addition to N. discophora, Booth (1966) included N. cial anatomy, and colony characteristics closely re- mammoidea var. rubi, N. fuckeliana, N. lucida and N. semble Neo. discophora, but cultures lack conidia, westlandica. The new species Neo. betulae, Neo. du- even when freshly isolated. Nectria fuckeliana is re- montii and Neo. viridispora can be added to these. ported to produce a Cylindrocarpon anamorph with Perithecia of Neo. betulae and Neo. dumontii are ana- abundant microconidia (Booth 1959, 1966, Roll-Han- tomically and biologically similar to those of Neo. dis- sen 1962). This species could be assigned to the Neo. cophora, but cultures of the former remained sterile coccinea Group due to its microconidial production and we have not had the opportunity to culture the and colony characteristics and by the fact that peri- latter. thecia of all ages occur in a single cluster (Booth Perithecia of all of these species are red. They of- 1959, 1966), but it is included here because of its N. ten are yellow or orange when young, darkening to mammoidea-like perithecial anatomy. red and brown, or sometimes near black with age and Taxa in this group occur on a wide range of living are red in KOH and yellow in lactic acid. or recently dead, woody plant substrata, including Members of the N. mammoidea Group most dis- palms, gymnosperms and dicotyledonous plants; less tinctively possess characteristic perithecial walls. In frequently they occur on herbaceous tissue. Neonec- longitudinal section the wall is seen to comprise a tria discophora var. rubi is known only from Rubus layer of hyphae that have thickened walls and typi- species where it causes a canker. Perithecia are typi- cally are arranged radially, giving the appearance of cally super®cial, solitary or clustered on a character- a palisade (Booth 1959; FIGS. 17, 24, 36, 44, 60). This istic, weakly developed basal stroma as was described wall structure appears in squash mounts as an inter- above. Perithecia typically do not collapse when dry twined layer of thickened hyphal elements, rather but sometimes become cupulate. than as a pseudoparenchymatous structure. As a re- To test the monophyly of Cylindrocarpon and Neo- sult of the uniform palisade layer, the perithecia of nectria we sequenced the mit ssu rDNA gene for rep- N. discophora typically appear smooth and shining resentative species. This expands work reported by Mantiri et al (2001) for Cylindrocarpon and Neonec- (see FIGS. 5, 6) but, in some collections or species, tria. an additional outer layer of globose cells covering the perithecia gives a roughened,
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