Cylindrocladiella

Boesew., Canad. J. Bot. 60: 2289. 1982. Fig. 4.

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Fig. 4. Cylindrocladiella spp. A–D. Conidiophores of Cylindrocladiella spp. on infected alfalfa seeds A–B. Cylindrocladiella spp. sporulating on the seed coat of Medicago sativa. C. Root rot of M. sativa seedling. D. Cylindrocladiella spp. on carnation leaf. E–AA. Asexual morph. E–I. Penicillate conidiophores. E. Cylindrocladiella longistipitata (ex-type CBS 116075). F. Cylindrocladiella kurandica (ex-type CBS 129577). G. Cylindrocladiella lanceolata (ex-type CBS 129566). H. Cylindrocladiella pseudoparva (ex-type CBS 129560). I. Cylindrocladiella nederlandica (ex-type CBS 152.91). J–N. Penicillate conidiogenous apparatus. J. Cylindrocladiella hawaiiensis (ex-type CBS 129569). K. Cylindrocladiella australiensis (ex-type CBS 129567). L. Cylindrocladiella natalensis (ex-type CBS 114943). M. Cylindrocladiella cymbiformis (ex-type CBS 129553). N. Cylindrocladiella ellipsoidea (ex-type CBS 129573). O–S. Subverticillate conidiophores. O. Cylindrocladiella australiensis (ex-type CBS 129567). P. Cylindrocladiella longiphialidica (ex-type CBS 129557). Q. Cylindrocladiella pseudohawaiiensis (ex-type CBS 210.94). R, S. Cylindrocladiella natalensis (ex-type CBS 114943). T–Y. Terminal vesicles of stipe extensions. T. Cylindrocladiella hawaiiensis (ex-type CBS 129569). U. Cylindrocladiella stellenboschensis (ex-type CBS 110668). V. Cylindrocladiella cymbiformis (ex-type CBS 129553). W. Cylindrocladiella variabilis (ex-type CBS 129561). X. Cylindrocladiella lanceolata (ex-type CBS 129566). Y. Cylindrocladiella kurandica (ex-type CBS 129577). Z, AA. Conidia. Z. Cylindrocladiella natalensis (ex-type CBS 114943). AA. Cylindrocladiella brevistipitata (ex-type CBS 142783). Scale bars: E–I, O = 50 μm; J–N, P–AA = 10 μm.

Synonym: Nectricladiella Crous & C.L. Schoch, Stud. Mycol. 45: 54. 2000.

Classification: Sordariomycetes, Hypocreomycetidae, Hypocreales, Nectriaceae.

Type species: Cylindrocladiella parva (P.J. Anderson) Boesew., basionym: Cylindrocladium parvum P.J. Anderson. Representative strain: CBS 114524 = ATCC 28272.

DNA barcodes (genus): LSU, ITS.

DNA barcodes (species): his3, tef1, tub2. Table 3. Fig. 5.

Table 3. DNA barcodes of accepted Cylindrocladiella spp.

Species	Isolates1	GenBank accession numbers2					References
		ITS	LSU	his3	tef1	tub2
Cylindrocladiella addiensis	CBS 143794T	MH111383	–	–	MH111393	MH111388	Present study
	CBS 143793	MH111385	–	–	MH111395	MH111390	Present study
	CBS 143795	MH111384	–	–	MH111394	MH111389	Present study
C. australiensis	CBS 129567T	JN100624	JN099222	JN098932	JN099060	JN098747	Lombard et al. (2012)
C. brevistipitata	CBS 142786T	–	–	–	MF444940	MF444926	Lombard et al. (2017)
C. camelliae	IMI 346845	AF220952	JN099249	AY793509	JN099087	AY793471	Van Coller et al., 2005, Lombard et al., 2012
C. clavata	CBS 129564T	JN099095	JN099135	JN098858	JN098974	JN098752	Lombard et al. (2012)
C. cymbiformis	CBS 129553T	JN099103	JN099143	JN098866	JN098988	JN098753	Lombard et al. (2012)
C. elegans	CBS 338.92T	AY793444	JN099201	AY793512	JN099039	AY793474	van Coller et al. (2005), Lombard et al. (2012)
C. ellipsoidea	CBS 129573T	JN099094	JN099134	JN098857	JN098973	JN098757	Lombard et al. (2012)
C. hahajimaensis	MAFF 238172T	JN687561	–	–	JN687562	–	Inderbitzin et al. (2012)
C. hawaiiensis	CBS 129569T	JN100621	JN099219	JN098929	JN099057	JN098761	Lombard et al. (2012)
C. horticola	CBS 142784T	MF444911	–	–	MF444938	MF444924	Lombard et al. (2017)
C. humicola	CBS 142779T	MF444906	–	–	MF444933	MF444919	Lombard et al. (2017)
C. infestans	CBS 111795T	AF220955	JN099199	AY793513	JN099037	AF320190	Schoch et al., 2000, Crous et al., 2001, van Coller et al. (2005), Lombard et al. (2012)
C. kurandica	CBS 129577T	JN100646	JN099245	JN098953	JN099083	JN098765	Lombard et al. (2012)
C. lageniformis	CBS 340.92T	AF220959	JN099165	AY793520	JN099003	AY793481	Schoch et al. (2000), van Coller et al. (2005), Lombard et al. (2012)
C. lanceolata	CBS 129566T	JN099099	JN099139	JN098862	JN098978	JN098789	Lombard et al. (2012)
C. lateralis	CBS 142788T	MF444914	–	–	MF444942	MF444928	Lombard et al. (2017)
C. longiphialidica	CBS 129557T	JN100585	JN099264	JN098851	JN098966	JN098790	Lombard et al. (2012)
C. longistipitata	CBS 116075T	AF220958	JN099155	AY793546	JN098993	AY793506	Schoch et al. (2000), van Coller et al. (2005), Lombard et al. (2012)
C. microcylindrica	CBS 111794T	AY793452	JN099203	AY793523	JN099041	AY793483	van Coller et al. (2005), Lombard et al. (2012)
C. natalensis	CBS 114943T	JN100588	JN099178	JN098895	JN099016	JN098794	Lombard et al. (2012)
C. nederlandica	CBS 152.91T	JN100603	JN099195	JN098910	JN099033	JN098800	Lombard et al. (2012)
C. novazelandica	CBS 486.77T	AF220963	JN099212	AY793525	JN099050	AY793485	Schoch et al. (2000), van Coller et al. (2005), Lombard et al. (2012)
C. nauliensis	CBS 143792T	MH111387	–	–	MH111397	MH111392	Present study
	CBS 143791	MH111386	–	–	MH111396	MH111391	Present study
C. parva	CBS 114524	AF220964	JN099171	AY793526	JN099009	AY793486	Schoch et al. (2000), van Coller et al. (2005), Lombard et al. (2012)
C. peruviana	IMUR 1843T	AF220966	JN099266	AY793540	JN098968	AY793500	Schoch et al. (2000), van Coller et al. (2005), Lombard et al. (2012)
C. pseudocamelliae	CBS 129555T	JN100577	JN099256	JN098843	JN098958	JN098814	Lombard et al. (2012)
C. pseudohawaiiensis	CBS 210.94T	JN099128	JN099174	JN098890	JN099012	JN098819	Lombard et al. (2012)
C. pseudoinfestans	CBS 114531T	AF220957	JN099166	AY793548	JN099004	AY793508	Schoch et al. (2000), van Coller et al. (2005), Lombard et al. (2012)
C. pseudoparva	CBS129560T	JN100620	JN099218	JN098927	JN099056	JN098824	Lombard et al. (2012)
C. queenslandica	CBS 129574T	JN099098	JN099098	JN098861	JN098977	JN098826	Lombard et al. (2012)
C. reginae	CBS 142782T	MF444909	–	–	MF444936	MF444922	Lombard et al. (2017)
C. stellenboschensis	CBS 110668T	JN100615	JN099213	JN098922	JN099051	JN098829	Lombard et al. (2012)
C. terrestris	CBS 142789T	MF444915	–	–	MF444943	MF444929	Lombard et al. (2017)
C. thailandica	CBS 129571T	JN100582	JN099261	JN098848	JN098963	JN098834	Lombard et al. (2012)
C. variabilis	CBS 129561T	JN100643	JN099242	JN098950	JN099080	JN098719	Lombard et al. (2012)
C. viticola	CBS 112897T	AY793468	JN099226	AY793544	JN099064	AY793504	van Coller et al. (2005), Lombard et al. (2012)
C. vitis	CBS 142517T	KY979751	KY979806	–	KY979891	KY979918	Crous et al. (2017a)

1

CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; IMI: International Mycological Institute, CABI-Bioscience, Egham, Bakeham Lane, U.K; IMUR: Institute of Mycology, University of Recife, Recife, Brazil; MAFF: Genetic Resources Centre, National Agriculture and Food Research Organization (NARO), NARO Genebank, Ibaraki, Japan. ^T indicates ex-type strains.

2

ITS: internal transcribed spacers and intervening 5.8S nrDNA; LSU: 28S large subunit nrDNA; his3: partial histone H3 gene; tef1: partial translation elongation factor 1-alpha gene; tub2: partial β-tubulin gene.

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Fig. 5. The Maximum Likelihood (ML) consensus tree of Cylindrocladiella spp. inferred from the combined ITS (547 bp), tef1 (527 bp) and tub2 (502 bp) sequence alignment. Thickened lines indicate branches present in the ML, Maximum parsimony (MP) and Bayesian consensus trees. Branches with ML-bootstrap (BS) & MP-BS = 100 % and posterior probabilities (PP) = 1.00 are in blue. Branches with ML-BS & MP-BS ≥ 75 % and PP ≥ 0.95 are in green. The scale bar indicates 0.02 expected changes per site. The tree is rooted to Gliocladiopsis sagariensis CBS 199.55. Ex-type strains are indicated in bold. GenBank accession numbers are indicated in Table 3 and in Lombard et al., 2012, Lombard et al., 2017. TreeBASE: S22340.

Ascomata perithecial, superficial, solitary, basal stroma absent, globose to obpyriform, collapsing laterally when dry, smooth, with minute, brown setae arising from ascomatal wall surface, red, changing colour in KOH, ostiole consisting of clavate cells, lined with inconspicuous periphyses. Asci unitunicate, 8-spored, cylindrical, sessile, thin-walled, with a flattened apex, and a refractive apical apparatus. Ascospores uniseriate, overlapping, hyaline, ellipsoid to fusoid with obtuse ends, smooth, 1-septate. Conidiophores monomorphic, penicillate, or dimorphic (penicillate and subverticillate), mononematous, hyaline. Penicillate conidiophores consist of a stipe, a penicillate arrangement of fertile branches, a stipe extension, and a terminal vesicle. Subverticillate conidiophores consist of a stipe, and one or two series of phialides. Stipe septate, hyaline, smooth. Stipe extensions aseptate, straight, thick-walled, with one basal septum, terminating in a thin-walled vesicle of characteristic shape. Conidiogenous apparatus with primary branches 0–1-septate, secondary branches aseptate, terminating in 2–4 phialides. Phialides cylindrical, straight or doliiform to reniform to cymbiform, hyaline, aseptate, apex with minute periclinal thickening and collarette. Conidia cylindrical, rounded at both ends, straight, (0–)1(–3)-septate, frequently slightly flattened at base, held in asymmetrical clusters by hyaline slime. Chlamydospores brown, thick-walled, more frequently arranged in chains than clusters (adapted from Boesewinkel 1982 and Lombard et al. 2012).

Culture characteristics: Colonies on MEA white to pale brick when young, becoming pale brick to dark sepia when mature, fluffy, cottony, effuse to convex with papillate surface, margin entire, undulate, lobate, or fimbriate, sometimes with abundant chlamydospores forming microsclerotia within medium.

Optimal media and cultivation conditions: CLA to induce sporulation of the asexual morph at 25 °C, while for the sexual morph sterile toothpicks placed on SNA is used at 20 °C.

Distribution: Worldwide.

Hosts: Soil-borne, weak pathogen of forestry, agricultural and horticultural crops (Crous, 2002, Lombard et al., 2012).

Disease symptoms: Leaf spots, cutting rot, stem cankers, damping-off and root rot.

Notes: Boesewinkel (1982) established the asexual genus Cylindrocladiella, based on C. parva, to accommodate several cylindrocladium-like species characterised by small (<20 μm long), 1-septate, cylindrical conidia and aseptate stipe extensions. Initially, Cylindrocladiella spp. were linked to the sexual genus Nectricladiella (Crous and Wingfield, 1993, Schoch et al., 2000). Following the implementation of the International Code of Nomenclature for algae, fungi and plants (ICN; McNeill et al. 2012), Rossman et al. (2013) proposed that the generic name Cylindrocladiella be retained over Nectricladiella. Recently, Lombard et al. (2015) showed that the genus Cylindrocladiella formed a monophyletic group in the Nectriaceae, closely related to the genera Aquanectria and Gliocladiopsis. To date, 36 species of Cylindrocladiella have been recognised (Crous and Wingfield, 1993, Van Coller et al., 2005, Inderbitzin et al., 2012, Lombard et al., 2012, Lombard et al., 2015, Lombard et al., 2017, Crous et al., 2017a), of which two are linked to nectricladiella-like sexual morphs (Schoch et al., 2000, Crous, 2002, Lombard et al., 2012, Lombard et al., 2015). These fungi are generally soil-borne and regarded as saprobes or weak pathogens of numerous plant hosts (Crous, 2002, Van Coller et al., 2005, Scattolin and Montecchio, 2007, Lombard et al., 2012). Disease symptoms associated with Cylindrocladiella infection include leaf spots and root, stem and cutting rots (Crous et al., 1991b, Peerally, 1991, Crous and Wingfield, 1993, Crous, 2002, Van Coller et al., 2005, Scattolin and Montecchio, 2007, Lombard et al., 2012).

References: Boesewinkel 1982 (morphology and pathogenicity); Crous & Wingfield 1993 (morphology); Schoch et al., 2000, Lombard et al., 2012, Lombard et al., 2017 (morphology and phylogeny); Crous 2002 (morphology, pathogenicity and monograph); van Coller et al. 2005 (morphology, pathogenicity and phylogeny).

Cylindrocladiella addiensis

L. Lombard & Crous, sp. nov. MycoBank MB824497.

Etymology: Name refers to Addis Ababa, Ethiopia, from where this fungus was collected.

Cultures sterile. Cylindrocladiella addiensis differs from its closest phylogenetic neighbours, C. elegans and C. noveazelandica, by unique fixed alleles in three loci based on the alignments deposited in TreeBASE (S22340): ITS position 92(T); tef1 positions 32(T), 80(C), 84(C), 154(indel), 155(A), 156(G), 157(indel), 199(A), 244(G), 261(G), 368(T), 398(T), 458(G/C), 466(G), 467(C), 475(T), 478(C), 483(T), 485(T), 487(T), 490(T) and 492(G); tub2 position 174(indel).

Culture characteristics: Colonies convex, cottony, with smooth margins, cream; reverse pale luteous; chlamydospores not seen; reaching 45–65 mm after 1 wk on MEA at 24 °C in ambient light.

Materials examined: Ethiopia, Addis Ababa, from soil, 2010, coll. P.W. Crous, isol. L. Lombard [holotype CBS 143794 (maintained as metabolically inactive culture), isotype cultures CBS 143793, CBS 143795 (also maintained as metabolically inactive cultures).

Note: None of the three isolates of C. addiensis could be induced to sporulate on MEA, PDA, OA, SNA or SNA amended with carnation leaf pieces.

Cylindrocladiella nauliensis L. Lombard & Crous, sp. nov. MycoBank MB824500. Fig. 6.

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Fig. 6. Cylindrocladiella nauliensis (ex-type CBS 143792). A–D. Penicillate conidiophores. E–H. Penicillate conidiogenous apparatus. I–L. Terminal vesicles of stipe extensions. M, N. Subverticillate conidiophores. O. Conidia. Scale bars: A–D = 50 μm; E–O = 10 μm.

Etymology: Name refers to the area Aek Nauli, Indonesia, from where this fungus was collected.

Conidiophores 35–55 × 3–6 μm, dimorphic, penicillate and subverticillate, mononematous and hyaline, comprising a stipe, a penicillate arrangement of fertile branches, a stipe extension and a terminal vesicle; stipe septate, hyaline, smooth; stipe extension 100–135 μm long, 4–5 μm wide, aseptate, straight, thick-walled with one basal septum, terminating in thin-walled, broadly clavate to ellipsoidal vesicles sometimes with papillate apex. Penicillate conidiogenous apparatus 10–22 × 2–4 μm, with primary branches aseptate, secondary branches 8–15 × 2–4 μm, aseptate, each terminal branch producing 2–4 phialides; phialides 8–13 × 2–3 μm, elongate doliiform to reniform to cymbiform, hyaline, aseptate, apex with minute periclinal thickening and collarette. Subverticillate conidiophores abundant, comprised of a septate stipe and rarely primary branches terminating in 2–4 phialides; primary branches 25–45 × 2–4 μm, straight, hyaline, 0–1-septate; phialides 12–32 × 2–3 μm, cymbiform to cylindrical, hyaline, aseptate, apex with minute periclinal thickening and collarette. Conidia (10–)11–13(–14) × 2–3 μm (av. = 12 × 2 μm), cylindrical, rounded at both ends, straight, 1-septate, frequently slightly flattened at base, held in asymmetrical clusters by hyaline slime. Sexual morph unknown.

Culture characteristics: Colonies convex, cottony, with smooth margins, cream with pale luteous to brick centre; reverse pale luteous to honey with sepia centre; chlamydospores moderate throughout medium arranged in chains; reaching 60–70 mm after 1 wk on MEA at 24 °C in ambient light.

Materials examined: Indonesia, Sumatra Utara, Aek Nauli, from soil, May 2005, coll. M.J. Wingfield, isol. L. Lombard (holotype CBS H-23400, culture ex-type CBS 143792), isotype culture CBS 143791 (metabolically inactive).

Notes: Cylindrocladiella nauliensis is closely related to C. longistipitata. The stipe extensions of C. nauliensis (up to 135 μm long) are shorter than those of C. longistipitata (up to 216 μm long; Lombard et al. 2012). Additionally, the conidia of C. nauliensis are smaller [(10–)11–13(–14) × 2–3 μm (av. = 12 × 2 μm)] than those of C. longistipitata [(12–)14–16(–17) × 2–4 μm (av. = 15 × 3 μm); Lombard et al. 2012].

Authors: L. Lombard & P.W. Crous