Colletotrichum: complex species or species ... - CBS - KNAW

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Damm et al. to olivaceous grey, filter paper Anthriscus stem and medium partly covered with felty white aerial mycelium (and salmon acervuli), reverse same colours; growth rate 17.5–21.5 mm in 7 d (28.5–31.5 mm in 10 d). Colonies on OA flat with entire margin; surface honey, isabelline to olivaceous, almost entirely covered by felty white to pale olivaceous grey aerial mycelium, reverse buff, olivaceous, pale olivaceous grey, olivaceous grey to iron-grey, growth rate 16–18 mm in 7 d (26–29 mm in 10 d). Conidia in mass salmon. Material examined: Colombia, Cundinamarca, from fruit anthracnose of Solanum betaceum, 13 Aug. 2010, J. Molina, (CBS H-20726 holotype, culture ex-type CBS 129814 = T.A.6); Cundinamarca, from anthracnose on a fruit of Solanum betaceum, 13 Aug. 2010, J. Molina, culture CBS 129811 = T.A.3; Antioquia, Santa Rosa, from a flower of Solanum betaceum, 1998, collector unknown, CBS H-20728, culture CBS 129955 = Tom-12. Notes: Afanador-Kafuri et al. (2003) identified several strains from tamarillo in Colombia as C. acutatum, three of which are included in this study. Sreenivasaprasad & Talhinhas (2005) recognised these strains as a separate molecular group, A8, closely related to A1 (C. lupini). Colletotrichum tamarilloi can be separated from other species using CHS-1, HIS3, TUB2 and GAPDH sequences, most effectively with GAPDH, and forms a uniform cluster even with six genes (Fig. 1). Afanador-Kafuri et al. (2003) observed uniformity of banding patterns with apPCR, RAPD-PCR and A+T-rich DNA analyses of the strains they studied. They speculated that selection for clonality and homogeneity had occurred among the isolates, all of which were collected in one region in Colombia where only one cultivar of the host was cultivated. Conidia of C. tamarilloi are uniformly fusiform on SNA, and almost so on Anthriscus stem, while C. lupini forms conidia that are usually clavate on SNA and cylindrical on the stems. Additionally, we found that appressoria of C. lupini have an undulate to lobate margin, while those of C. tamarilloi have an entire or rarely slightly undulate edge. This species is only known on Solanum betaceum in Colombia. There are no previously described species associated with this host. Three Colletotrichum species are reported from tamarillo in the USDA fungal databases (Farr & Rossman 2012): C. acutatum (Guerber et al. 2003, Gadgil 2005) and C. gloeosporioides (Gadgil 2005) in New Zealand and C. simmondsii in Australia (Shivas & Tan 2009). None of these species/groups is identical with C. tamarilloi. While C. lupini and C. tamarilloi form well-supported clusters, there are several additional species and unnamed strains from various hosts in Central and South America, as well as in Florida that are closely related to C. lupini and C. tamarilloi. One of these is from tamarillo in the same locality in Colombia (CBS 129810). A recently reported anthracnose pathogen of tamarillo in the USA (Jones & Perez 2012) probably belongs to C. fioriniae according to its ITS sequence (JN863589). The Colletotrichum strains available to us from tamarillo in Colombia and New Zealand belong to C. godetiae, C. tamarilloi and an unnamed strain related to C. tamarilloi (this study), as well as C. boninense, C. constrictum and C. karstii belonging to the C. boninense species complex (Damm et al. 2012, this issue). Yearsley et al. (1988) report C. acutatum (s. lat.) infections of tamarillo in New Zealand; however none of our tamarillo strains isolated from New Zealand belongs to the C. acutatum group. The strains from this host included in Guerber et al. (2003) and assigned to group F2 formed a clade with strains described as C. johnstonii in this study. We did not find any species on tamarillo occurring in both Colombia and New Zealand. Falconi & van Heusden (2011) studied Colletotrichum isolates collected from Lupinus mutabilis and tamarillo in the Ecuadorian Andes. They formed two different subgroups within C. acutatum based on ITS sequence data. The isolates from lupins were pathogenic to tamarillo and vice versa, but lupin and tamarillo isolates were each more virulent to their own hosts. ITS sequence of the ex-type strain of C. tamarilloi, CBS 129814, matched with 100 % identity with JN543070 from isolate Tam7 from tamarillo, as well as JN543066 from isolate Lup28 from L. mutabilis in Ecuador (Falconi et al. 2012). The closest TUB2 blastn matches for CBS 129814 (with 99 % identity, 4 bp differences) were FN611029 and FN611028 from isolates DPI and CS-1 from Citrus aurantifolia and Citrus sinensis from USA, Florida (Ramos et al. 2006). The closest GAPDH matches (with 97 % identity) were EU647323 from leatherleaf fern and EU168905, EU647318 and EU647319 from sweet orange isolates, all from Florida, USA (Peres et al. 2008, MacKenzie et al. 2009). Colletotrichum walleri Damm, P.F. Cannon & Crous, sp. nov. MycoBank MB800517. Fig. 32. Etymology: Named after J.M. Waller, tropical pathologist extraordinaire and a key worker on the most important Colletotrichum pathogen of coffee. Sexual morph not observed. Asexual morph on SNA. Vegetative hyphae 1–6 µm diam, hyaline, smooth-walled, septate, branched. Chlamydospores not observed. Conidiomata not developed, conidiophores formed directly on hyphae. Setae not observed. Conidiophores hyaline, smooth-walled, septate, branched, to 70 µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical to ampulliform, 10–14 × 3–4 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm long, periclinal thickening distinct. Conidia hyaline, smooth-walled, aseptate, straight, cylindrical to fusiform with both ends slightly acute or one end round, (6–10.5)15.5–(–19.5) × (3–)3.5–4.5(–5.5) µm, mean ± SD = 13.0 ± 2.7 × 4.0 ± 0.5 µm, L/W ratio = 3.3. Appressoria single, medium brown, smooth-walled, elliptical, clavate, sometimes irregularly shaped, the edge entire or undulate, (4.5–)5.5–12.5(–18.5) × (3.5–)4.5–7.5(–10.5) µm, mean ± SD = 9.0 ± 3.3 × 5.9 ± 1.4 µm, L/W ratio = 1.5. Asexual morph on Anthriscus stem. Conidiomata either not developed, conidiophores formed directly on hyphae, or acervular, conidiophores formed on pale brown, angular, basal cells 3.5–7 µm diam. Setae not observed. Conidiophores hyaline to pale brown, smooth-walled, septate, branched, to 70 µm long. Conidiogenous cells hyaline to pale brown, smooth-walled, cylindrical, 12–23 × 2.5–3 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm long, periclinal thickening visible to distinct. Conidia hyaline, smoothwalled, aseptate, straight, sometimes slightly curved, cylindrical to fusiform with both ends ± acute or one end round, (10.5–)12–16(– 18.5) × 3.5–4(–4.5) µm, mean ± SD = 13.9 ± 1.8 × 4.0 ± 0.3 µm, L/W ratio = 3.5. Culture characteristics: Colonies on SNA flat with entire margin, hyaline, filter paper pale olivaceous grey, medium, filter paper and Anthriscus stem covert with fely white aerial mycelium, reverse same colours; 21–24 mm in 7 d (31–34 mm in 10 d). Colonies on OA flat with entire margin; surface covert with felty or short floccose white to pale olivaceous grey aerial mycelium, reverse olivaceous grey to iron grey, olivaceous in the centre and white towards the margin; 20–26 mm in 7 d (30.5–37.5 mm in 10 d). Conidia in mass salmon. 106
The Colletotrichum acutatum species complex Fig. 32. Colletotrichum walleri (from ex-holotype strain CBS 125472). A–B. Conidiomata. C–H. Conidiophores. I–N. Appressoria. O–P. Conidia. A, C–E, O. from Anthriscus stem. B, F–N, P. from SNA. A–B. DM, C–P. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–P. Material examined: Vietnam, Buon Ma Thuot-Dak Lac, from leaf tissue of Coffea arabica, unknown collection date, H. Nguyen, (CBS H-20795 holotype, culture extype CBS 125472 = BMT(HL)19). Notes: Species of the C. gloeosporioides species complex are well-known as pathogens of Coffea, especially the African coffee berry disease pathogen C. kahawae (Waller et al. 1993). Additional Coffea-associated components of this species complex from Vietnam and Thailand have been studied by Nguyen et al. (2009) and Prihastuti et al. (2009); see Weir et al. (2012, this issue) for further review. Masaba & Waller (1992) commented that strains identified as C. acutatum may cause minor disease of ripening coffee berries. Kenny et al. (2006) and Nguyen et al. (2010) respectively isolated, in Papua New Guinea and Vietnam, taxa in this species complex from coffee leaves, twigs and fruits. None of the Vietnamese isolates could infect undamaged coffee berries (Nguyen et al. 2010). One of the C. acutatum cultures studied by Nguyen et al. (BMT(HL)19) was sent to CBS and a dried sample of this strain is here designated as holotype of C. walleri. In this study, this is the only coffee isolate from Asia, while six other isolates from coffee, originating from Africa and Central America, belong to three other species within the C. acutatum species complex (C. fioriniae, C. acutatum s. str. and C. costaricense). Two of these strains were included in the study by Waller et al. (1993). Colletotrichum walleri is separated from other species by almost all genes. It is most easily distinguished using HIS3 and ITS sequences, while sequences of other genes differ by only one bp from those of other species. The CHS-1 sequence is the same as that of C. sloanei. The closest TUB2 blastn match for CBS 125472 (with 99 % identity, 5 bp differences) was GU246633 from isolate R14 from Capsicum annuum from South Korea (Sang et al. 2011). The closest GAPDH match for a sequence covering ± the full gene length (with 98 % identity, 4 bp differences) was HQ846724 from isolate OBP6 from an unnamed plant, probably from India (Chowdappa P, Chethana CS, Madhura S, unpubl. data). The only 100 % match with the ITS sequence was FJ968601, the sequence of the same isolate previously sequenced by Nguyen et al. (2009). DISCUSSION Colletotrichum acutatum (in the broad sense) was originally distinguished using morphological characteristics. The primary diagnostic feature was given as the possession of fusiform conidia with acute ends (Simmonds 1965). More detailed research has however shown that this characteristic is not absolute; while most strains of species within the C. acutatum complex have at least a proportion of conidia with at least one acute end, it is common to find significant variation in conidial shape within species and even within individual strains. Conidia that are more or less cylindrical are frequently encountered. The variation may have multiple causes; in some circumstances it seems that secondary conidia www.studiesinmycology.org 107
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