ARTICLE 101 . . et in in in et al et al Ilex have (peanut), ), namely Calonectria Calonectria (as o 2: 101–108 Key words: Hypocreales Calonectria Cylindrocladium Ilex aquifolium TUB HIS systematics n Calonectria
· infections include Ilex aquifolium 1 (soybean) (Crous occur commonly in in Florida (USA); spp. in Georgia and Ilex paraguariensis me Aquifoliaceae Ilex paraguayensis . 2009, 2010a, d). Major on Clare Island (Ireland), Ilex Arachishypogea and ( on et al volu Ilex · on Calonectria 2010), as well as root rot and on Tetracytum Calonectria Glycine max , a pathogen gus C. ilicicola is proposed as Ilex vomitoria n et al. Cylindrocladiumilicicola Ilexaquifolium , based on IMA Fu Ca. ilicicola )on 2 Ca. canadiana Calonectria spathulata Ca. lauri Over the past few years, a species of Most species of . 1993, Wright soil, especially the in world. subtropical Although the genusas to was saprobic tropicaloriginally regarded regions (Gravesproven to of 1915), be importantwith taxa a have plant wide pathogens, sincesymptoms host been ranging range associated of fromdamping plants,off, leaf cutting spots causingrot, root to and stem disease fruit rot cankers, (Crous was collected France. from Presently leavesbeen four species described of of from 2004b, 2006a). diseases attributed Cylindrocladium to black rot of and red crown rot of al leaf diseases of numerous diverse hosts (Crous 2004b, 2006a, Lombard Argentina, and Calonectria morganii Calonectria avesiculataFlorida(USA), pyrochroa and is distinct from leaves from France. Based on DNA sequence species occurring on leaves of Ilex . 2006a) , a genus . 1998) and , which is a Nectriaceae et al Calonectria lauri . On the host and in culture, yellow to brownish-yellow . 2000). Other . et al Cylindrocladium Cylindrocladium (2009, 2010a–d) , were shown to represent two distinct species, as the latter -like species with et al and Johannes Z. Groenewald 2 Xenocylindrocladium (Crous . 2010a–c). name for the genus, . 2005). Following the Calonectria et al. C. ilicicola et al are common saprobes and plant pathogens on a wide range of hosts ) (Lombard 2010a–c). et al Calonectria Cylindrocladiella is easily distinguished , which is a nursery pathogen involved with root rot of several tree genera collections obtained on (2006b, 2008, 2009a, b) with Ca. pyrochroa are members of Calonectria Curvicladiella Cylindrocladium (Crous Calonectria et al. Cylindrocladium ilicicola n in Europe , Pedro W. Crous Calonectria o 1 You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). the of use your or you endorse they that suggests that way any in not (but licensor or author the by specified manner the in work the attribute must You may not use this work for commercial purposes. You transform, or build upon this work. may not alter, You Calonectria anamorphs. Formerly ti teleomorphs (Schoch Ascomycetes . 1997), , -tubulin and histone gene regions, as well as morphology, the new collections matched Cy. canadiense Calonectria b are characterised by having uniloculate, Submitted: 1 September 2010; Accepted: 29 September 2010; Published: 2 November 2010. Species of
et al
1999). is subsequently proposed for Dematiocladium roduc
nt Hypocreales CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands AscoFrance, 64 route de Chizé, F-79360, Villiers en Bois, France; corresponding author e-mail: [email protected] Nectricladiella separatedfromthiscomplex include morphologicallysimilar genera that have also since been (Decock and approach of Crous other fungal groups, Lombard monophyletic genus (Lombard taxa are since accommodated in chlamydospore-like synanamorph was observed. All chose to use the older irrespective whether the teleomorphanamorph, or unnamed microconidial, megaconidial, or its purported teleomorph,has bright red perithecia that strain purple in KOH. A new combination, perithecia were observed that did not strain red in 3 % KOH. Based on these results, the status of new occurring in subtropical to tropical regions of datathe ofworld. their The aim of thethe ex-typepresent strainstudy wasof to resolve Abstract: lauri, commonly associated with Cylindrocladium black rot of peanut. Finally, new name for Article info: in Quebec, Canada. You are free to share - to copy, distribute and transmit the work, under the following conditions: distribute and transmit the work, under the following are free to share - to copy, You Attribution: © 2010 International Mycological Association © 2010 International Mycological Non-commercial: No derivative works: For any reuse or distribution, you must make clear to others the license terms of this work, which can be found Nothing in this license impairs or restricts the author’s moral rights. at permission from the copyright holder. http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get
Species of I ( Nectriaceae et al. orange to purple, superficial ascomata (Rossman Cylindrocladium from other members of the family based on its
also included members of small conidia (Boesewinkel 1982, Victor aquifolium 2 1 Christian Lechat The enigma of that accommodates volume 1 · no. 2 Lechat et al.
Brazil (Crous 2002). Hawksworth & Sivanesan (1976) 3’ end of the 18S nrRNA gene (SSU), the first internal also reported a Calonectria species on Ilex aquifolium transcribed spacer (ITS1), the 5.8S nrRNA gene, the from Slapton, South Devon, England, which appears second ITS region (ITS2) and the 5’ end of the 28S to be undescribed, with ascospores 3-septate, 14–22 nrRNA gene (LSU) was amplified for some isolates as ×3–4 µm. The collection obtained from France and explained in Lombard et al. (2010c). The generated ARTICLE treated in this study, is morphologically distinct from sequences were compared with other fungal DNA taxa presently reported from Ilex. sequences from NCBI’s GenBank sequence database In recent years there have been several revisions using a blastn search; TUB sequences with high focused on either Calonectria or its anamorph similarity were added to the alignment and the result of genus, Cylindrocladium (Rossman 1979, Peerally sequences of the other loci were used as confirmation 1991, Crous & Wingfield 1994, Crous 2002). The (not shown). The additional GenBank sequences were first attempt to provide a molecular phylogeny of the manually aligned using Sequence Alignment Editor genus was that of Schoch et al. (2001) based on v. 2.0a11 (Rambaut 2002). Phylogenetic analyses b-tubulin DNA sequences. This gene region, however, of the aligned sequence data were performed using proved insufficiently variable to reliably distinguish all PAUP (Phylogenetic Analysis Using Parsimony) v. species complexes in the genus (Kang et al. 2001a, 4.0b10 (Swofford 2003) and consisted of neighbour- b, Henricot & Culham 2002, Crous et al. 2004b, joining analyses with the uncorrected (“p”), the Kimura 2006a). Since then, a concerted effort has been made 2-parameter and the HKY85 substitution models. to generate a multi-gene phylogeny for taxa in the Alignment gaps were treated as missing data and all genus, and identify the best suited gene for species characters were unordered and of equal weight. Any delimitation (Lombard et al. 2009, 2010a–d). Based ties were broken randomly when encountered. For on these findings, a combination of b-tubulin DNA parsimony analyses, alignment gaps were treated as a sequence data, supplemented with either calmodulin fifth character state and all characters were unordered or elongation factor 1-a, proved the most effective in and of equal weight. Maximum parsimony analysis distinguishing all known taxa. was performed using the heuristic search option with The aim of the present study was to compare the 100 random (ITS) or simple (LSU) taxa additions and new collections on Ilex from France to all species known tree bisection and reconstruction (TBR) as the branch- in the genus, using morphology and DNA sequence swapping algorithm. Branches of zero length were analysis of their b-tubulin and histone gene regions in collapsed and all multiple, equally parsimonious trees order to determine if it represented a novel taxon. were saved. The robustness of the trees obtained was evaluated by 1 000 bootstrap replications (Hillis & Bull 1993). Tree length (TL), consistency index Materials and methods (CI), retention index (RI) and rescaled consistency index (RC) were calculated. Sequences derived in this Isolates study were lodged at GenBank (
102 i m a f u n G U S Calonectria lauri sp. nov.
Collection details and GenBank accession numbers of isolates of Calonectria lauri included in this study. Table 1. ARTICLE
Strain No.1 Substrate Country Collector(s) GenBank Accession No. (TUB, HIS, ITS)2 CPC 15683 Leaves of Ilex aquifolium Netherlands W. Gams FR694682, FR694676, FR694679 CBS 126269 = CPC 17978 Leaves of I. aquifolium France A. Gardiennet FR694683, FR694677, FR694680 CBS 553.69 = IMI 299390 Root of Buxus sempervirens Belgium — FR694684, FR694678, — CBS 749.70 I. aquifolium Netherlands H.A. van der Aa FR694685, GQ267250, GQ280584 1CBS: CBS Fungal Biodiversity Centre, Utrecht, The Netherlands; CPC: Culture collection of P.W. Crous, housed at CBS; IMI: International Mycological Institute, CABI-Bioscience, Egham, Bakeham Lane, UK. 2TUB: partial beta-tubulin gene; HIS: partial histone H3 gene; ITS: Internal transcribed spacers 1 and 2 together with 5.8S nrDNA.
Results region, ostiole papillate, composed of palisade-like, cylindrical to narrowly ellipsoidal cells. Ascomatal wall Phylogeny 50–65 µm thick of two regions; outer region comprising Approximately 600, 480 and 680 bases were determined warts 50–55 µm thick, composed of globose to nearly for the isolates indicated in Table 1 for TUB, HIS and angular, thick-walled cells, 10–30 × 5–16 µm, yellow, ITS, respectively. Of the β-tubulin gene, 522 bases wall 1.5–2 µm thick; inner region 5–10 µm thick, were used for phylogenetic analyses in the manually composed of flattened, ellipsoidal cells, 12–18 × 3–5 adjusted alignment containing 32 isolates (including µm, hyaline; warts globose to subglobose 25–40 × 15– the outgroup sequence). Of these 522 characters 30 µm, yellow. Asci clavate, long stipitate, 110–130 × (including alignment gaps), 180 were parsimony- 17–22 µm, 8-spored, multiseriate. Ascospores narrowly informative, 47 were variable and parsimony- fusiform with rounded ends, lightly curved, guttulate, uninformative, and 295 were constant. Neighbour- hyaline, smooth, (53–)60–86(–89) × 6.5–8(–9) µm, joining analysis using the three substitution models, 3-septate, not conctricted at the septa or constricted as well as the parsimony analysis, yielded trees with when overmature. Conidiophores consisting of a exactly the same topologies. Parsimony analysis of stipe bearing a penicillate arrangement of fertile the alignment yielded a single most parsimonious tree branches, a stipe extension, and a terminal vesicle; (TL = 381 steps; CI = 0.816; RI = 0.953; RC = 0.778), stipe septate, hyaline, smooth, 40–150 × 3–5 µm; stipe which is shown in Fig. 1. extensions septate, straight to flexuous, 120–200 µm long, 2.5–3 µm wide at the apical septum, terminating Taxonomy in an obpyriform to ellipsoid vesicle, (5–) 7–8(–10) µm diam. Conidiogenous apparatus with primary Calonectria lauri (Vanderw.) Lechat & Crous, branches aseptate or 1-septate, 15–20 × 4–5 µm; comb. nov. secondary branches aseptate, 8–15 × 4–5 µm; tertiary MycoBank MB517423 branches aseptate, 10–15 × 4–5 µm, each terminal (Fig. 2) branch producing 2–4 phialides; phialides doliiform Basionym: Tetracytum lauri Vanderw., Parasitica 1: to reniform, hyaline, aseptate, 6–12 × 2.5–4 µm; apex 145. 1945. (as “laurii”). with minute periclinal thickening and inconspicuous = Candelospora ilicicola Hawley, Proc. Roy. Irish collarette. Conidia cylindrical, rounded at both ends, Acad. 31: 11. 1912. [non Calonectria ilicicola Boedijn & straight, (45–) 55–68(–73) × (4–)5–6(–7) µm (av. = 60 Reitsma, 1950] × 5.5 µm), (1–)3-septate, lacking a visible abscission = Cylindrocladium ilicicola (Hawley) Boedijn & Reitsma, scar, held in parallel cylindrical clusters by colourless Reinwardtia 1: 57. 1950. slime. Megaconidia and microconidia unknown.
Typus: Ireland, Clare Island, Ilex aquifolium, Hawley, K (M) Culture characteristics: Colonies on MEA sienna to 61269!, holotype of Cy. ilicicola, IMI 76542 isotype. Netherlands, brick on the surface, and sienna in reverse; sienna on South-East Limburg, Vijlenerbos, Vijlen, Ilex aquifolium, Aug. OA (surface); sienna to umber on PDA (surface), and 1970, H.A van der Aa, epitype CBS H-15110, ex-epitype culture umber in reverse; chlamydospores on MEA moderate, CBS 749.70. occurring throughout the medium, with sparse to moderate sporulation on aerial mycelium. Ascomata perithecial, solitary, scattered, subglobose to ovoid, 450–550 µm high × 380–420 µm diam, Additional specimens examined: Netherlands, Hilversum, superficial, not obviously stromatic but difficult to on leaves of Ilex aquifolium, 11 Nov. 2008, W. Gams, CPC remove from the subtratum because basal cells of 15683 = CBS 128031, CPC 15684, CPC 15685. France, ascomata remain immersed in the substratum, yellow to Pressigny (52), on leaves of Ilex aquifolium, 05 Dec. 2009, A. brownish-yellow, dark-red at base, not changing colour Gardiennet, AG09308, CBS H-20476, culture CPC 17978 = in 3 % KOH or lactic acid, warted except at ostiolar CBS 126269; Forêt de Chizé, Villiers en Bois (79) on leaves
volume 1 · no. 2 103 Lechat et al.
Cylindrocladiella lageniformis AY725652 DQ190564 100 DQ190557 Calonectria colhounii
ARTICLE 62 DQ190560 100 Calonectria pauciramosa AY078119 AF308466 66 100 Calonectria leucothoës AF308465 Calonectria citri AF333393 100 51 CPC 15683 CBS 749.70 100 CPC 17978 Calonectria lauri AY078122 CBS 553.69 84 AY078120 Calonectria “ilicicola” AY725641 Calonectria colombiensis GQ267207 53 Calonectria curvispora AF333395 90 GQ267213 Calonectria pacifica 100 AY725630
62 GQ267209 Calonectria kyotensis 77 GQ267208 76 AY725642 GU256586 99 GU256594 10 changes AY725631 AY725636 Calonectria ilicicola AY725637 AY725639 68 AY725643 AY725647 AY725646 AY725645
Fig. 1. Single most parsimonious trees obtained from a heuristic search with 100 random taxon additions of the β-tubulin sequence alignment. The scale bar shows 10 changes and bootstrap support values from 1000 replicates are shown at the nodes. The tree was rooted to Cylindrocladiella lageniformis (GenBank AY725652).
104 i m a f u n G U S Calonectria lauri sp. nov. ARTICLE
Fig. 2. Calonectria lauri and its Cylindrocladium anamorph. A, B. Yellowish perithecia in vivo (A), and in vitro (B). C. Cylindrocladium anamorph. D. Vertical section through perithecium, showing wall anatomy. E. Ascospores. F–H. Conidiophores. I–L. Conidiogenous apparatus with phialides. M. Ellipsoid to obpyriform vesicles. N. Three-septate conidia. Scale bars: A, B = 200 µm, C, E–H, M = 8 µm, D, J–L, N = 10 µm, I = 5.5 µm.
volume 1 · no. 2 105 Lechat et al.
of Ilex aquifolium, 19 Sept. 2006, C. Lechat, CLL696. Belgium, collection (on the host and on CLA in culture), forms Gent, on roots of Buxus sempervirens, July 1969, A. Roos, yellow to brownish yellow perithecia that do not IMI 299390 = CBS 553.69. discolour in KOH (except at the perithecial base). The teleomorph of C. ilicicola could therefore not be Notes: The name Calonectria ilicicola is already Ca. pyrochroa as currently accepted (Lombard et al. ARTICLE occupied, and thus the next available epithet for this 2010c). Because the name Ca. ilicicola is already species in Calonectria is that of Tetracytum lauri. occupied by the pathogen causing Cylindrocladium Calonectria lauri is phylogenetically closely related to black rot of peanut (Crous et al. 1993), a new name, Ca. citri (known on Citrus from Florida). Morphologically Ca. lauri, is proposed for this species, which appears the two species can be separated in that Ca. citri has to occur commonly on Laurus, Ilex, as well as several ellipsoid to pyriform or obovoid vesicles, and 3-septate other hosts in Europe (Brayford & Chapman 1987). conidia that are slightly shorter and narrower, (25–)53– Presently no cultures are available of Ca. pyrochroa, 60(–65) × 3–4(–5) µm (Crous 2002). and further collections will have to be made from Platanus leaf litter in France to help clarify the morphology of its Cylindrocladium anamorph. Discussion
The genus Calonectria is based upon Calonectria APPENDIX pyrochroa (on Platanus leaf litter, France, lectotype BPI), which Rossman (1979) found to be In the recent treatment of the genus Calonectria, indistinguishable from Ca. daldiniana (on Magnolia Lombard et al. (2010c) allocated the name grandiflora leaf litter, Italy, holotype RO). A separate Cylindrocladium canadense to Calonectria as Ca. collection from decaying leaves of Pittosporum canadensis (J.C. Kang, Crous & C.L. Schoch) L. undulatum collected in Madeira (CUP-MM 2407) Lombard, M.J. Wingf. & Crous, but overlooked the produced a Cylindrocladium anamorph with clavate older existing name, Ca. canadensis (Ellis & Everh.) vesicles, which later led Rossman (1983) to conclude Berl. & Voglino. A new combination is required to that the oldest anamorph epithet that could be linked resolve this homonym as follows: to Ca. pyrochroa was C. ilicicola. Brayford & Chapman (1987) reported a wilting Calonectria canadiana L. Lombard, M.J. Wingf. disease of Laurus nobilis in nurseries on the Isles & Crous, nom. nov. of Scilly, and later on Arbutus andrachnoides and MycoBank MB517424 Gaultheria shallon in West Devon, UK. The causal Basionym: Cylindrocladium canadense J.C. Kang, organism was identified as C. ilicicola, but incorrectly Crous & C.L. Schoch, Syst. Appl. Microbiol. 24: 210. linked to the teleomorph name, Ca. ilicicola. Based 2001. on a molecular comparison of ex-type strains, Crous = Calonectria canadensis (J.C. Kang, Crous & C.L. et al. (1993) showed Ca. ilicicola was the teleomorph Schoch) L. Lombard, M.J. Wingf. & Crous, Stud. Mycol. of C. parasiticum, a major pathogen associated with 66: 56. 2010, non Calonectria canadensis (Ellis & Everh.) Cylindrocladium black rot of peanut. In a later study, Berl. & Voglino, Addendum to Syll. Fung. 4: 212. 1886. Crous & Wingfield (1994) accepted the relationship between Ca. pyrochroa and C. ilicicola, as there were no cultures available at the time to refute this Acknowledgements proposed link (Crous 2002). Following a revision of Cylindrocladium strains in the CBS culture collection, The authors thank the technical staff, Arien van Iperen Crous et al. (2006a) discovered a strain linked to a (cultures), Marjan Vermaas (photo plates), and Mieke Starink- specimen that closely matched the type of C. ilicicola, Willemse (DNA isolation, amplification and sequencing) for and subsequently designated CBS 749.70 (on Ilex their invaluable assistance. Drew Minnis (USDA, Beltsville, aquifolium, the Netherlands) as ex-epitype strain for USA) is also thanked for bringing the homonym associated C. ilicicola. Sequence data derived from the ex-epitype with epithet “canadensis” to our attention. Finally, we thank strain, and morphology, proved to be identical to that Alain Gardiennet for the supply of specimens. of the new collection obtained from France (Figs 1–2), confirming it to be C. ilicicola. References However, isolate CBS 126269 produced a Calonectria teleomorph in culture, which is clearly Boesewinkel HJ (1982) Cylindrocladiella, a new genus to distinct from Ca. pyrochroa. The latter species (and accommodate Cylindrocladium parvum and other small- its synonyms) have scarlet-red perithecia, which turn spored species of Cylindrocladium. Canadian Journal of purple in 2 % KOH (Rossman 1979). The present Botany 60: 2288–2294.
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Brayford D, Chapman AU (1987) Cylindrocladium ilicicola on Hillis DM, Bull JJ (1993) An empirical test of bootstrapping ARTICLE cuttings of evergreen ornamental shrubs in the UK. Plant as a method for assessing confidence in phylogenetic Pathology 36: 413–414. analysis. Systematic Biology 42: 182–192. Crous PW (2002) Taxonomy and pathology of Cylindrocladium Kang JC, Crous PW, Old KM, Dubzinski MJ (2001a) Non- (Calonectria) and allied genera. APS Press, St. Paul. conspecificity of Cylindrocladium quinqueseptatum and Crous PW, Allegrucci N, Arambarri AM, Cazau MC, Calonectria quinqueseptata based on a β-tubulin gene Groenewald JZ, Wingfield MJ (2005) Dematiocladium phylogeny and morphology. Canadian Journal of Botany celtidis gen. sp. nov. (Nectriaceae, Hypocreales), a new 79: 1241–1247. genus from Celtis leaf litter in Argentina. Mycological Kang JC, Crous PW, Schoch CL (2001b) Species concepts Research 109: 833–840. in the Cylindrocladium floridanum and Cy. spathiphylli Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G complexes (Hypocreaceae) based on multi-allelic (2004a) MycoBank: an online initiative to launch mycology sequence data, sexual compatibility and morphology. into the 21st century. Studies in Mycology 50: 19–22. Systematic and Applied Microbiology 24: 206–217. Crous PW, Groenewald JZ, Risède J-M, Simoneau P, Hyde Lombard L, Crous PW, Wingfield BD, Wingfield MJ (2010a) KD (2006a) Calonectria species and their Cylindrocladium Species concepts in Calonectria (Cylindrocladium). anamorphs: species with clavate vesicles. Studies in Studies in Mycology 66: 1–14. Mycology 55: 213–226. Lombard L, Crous PW, Wingfield BD, Wingfield MJ (2010b) Crous PW, Groenewald JZ, Risède J-M, Simoneau P, Hywel-Jones Multigene phylogeny and mating tests reveal three cryptic NL (2004b) Calonectria species and their Cylindrocladium species related to Calonectria pauciramosa. Studies in anamorphs: species with sphaeropedunculate vesicles. Mycology 66: 15–30. Studies in Mycology 50: 415–430. Lombard L, Crous PW, Wingfield BD, Wingfield MJ (2010c) Crous PW, Slippers B, Wingfield MJ, Rheeder J, Marasas Phylogeny and systematics of the genus Calonectria. WFO, Phillips AJL, Alves A, Burgess T, Barber P, Studies in Mycology 66: 31–69. Groenewald JZ (2006b) Phylogenetic lineages in the Lombard L, Rodas CA, Crous PW, Wingfield BD, Wingfield MJ Botryosphaeriaceae. Studies in Mycology 55: 235–253. (2009) Calonectria (Cylindrocladium) species associated Crous PW, Summerell BA, Carnegie AJ, Wingfield with dying Pinus cuttings. Persoonia 23: 41–47. MJ, Groenewald JZ (2009a) Novel species of Lombard L, Zhou XD, Crous PW, Wingfield BD, Wingfield MJ Mycosphaerellaceae and Teratosphaeriaceae. Persoonia (2010d) Calonectria species associated with cutting rot of 23: 119–146. Eucalyptus. Persoonia 24: 1–11. Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ, Hunter Nirenburg HI (1981) A simplified method for identifying GC, Burgess TI, Andjic V, Barber PA, Groenewald JZ Fusarium spp. occurring on wheat. Canadian Journal of (2009b) Unravelling Mycosphaerella: do you believe in Botany 59: 1599–1609. genera? Persoonia 23: 99–118. O’Donnell K, Cigelnik E (1997) Two divergent intragenomic Crous PW, Verkley GJM, Groenewald JZ, Samson RA (eds) rDNA ITS2 types within a monophyletic lineage of (2009c) Fungal Biodiversity. [CBS Laboratory Manual the fungus Fusarium are nonorthologous. Molecular Series 1]. Centraalbureau voor Schimmelcultures, Phylogenetics and Evolution 7: 103–116. Utrecht. Peerally A (1991) The classification and phytopathology of Crous PW, Wingfield MJ (1994) A monograph of Cylindrocladium species. Mycotaxon 40: 367–366. Cylindrocladium, including anamorphs of Calonectria. Rambaut A (2002) Sequence Alignment Editor. Version 2.0. Mycotaxon 51: 341–435. Department of Zoology, University of Oxford, Oxford, Crous PW, Wingfield MJ, Alfenas A (1993) Cylindrocladium UK. Software distributed by author (
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Schoch CL, Crous PW, Wingfield MJ, Wingfield BD (2000) Wright LP, Davis AJ, Wingfield BD, Crous PW, Brenneman Phylogeny of Calonectria and selected hypocrealean T, Wingfield MJ (2010) Population structure of genera with cylindrical macroconidia. Studies in Mycology Cylindrocladium parasiticum infecting peanuts (Arachis 45: 45–62. hypogaea) in Georgia, USA. European Journal of Plant Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Pathology 127: 199–206. ARTICLE Parsimony (* and Their Methods). Version 4.0b.10 Sinauer Associates, Sunderland, Massachusetts. Victor D, Crous PW, Janse BJH, Zyl WH van, Wingfield MJ, Alfenas AC (1998) Systematic appraisal of . species complexes within the hyphomycete genus Cylindrocladiella. Mycological Research 102: 273–279.
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