Alternaria redefined

Abstract

Alternaria is a ubiquitous fungal genus that includes saprobic, endophytic and pathogenic species associated with a wide variety of substrates. In recent years, DNA-based studies revealed multiple non-monophyletic genera within the Alternaria complex, and Alternaria species clades that do not always correlate to species-groups based on morphological characteristics. The Alternaria complex currently comprises nine genera and eight Alternaria sections. The aim of this study was to delineate phylogenetic lineages within Alternaria and allied genera based on nucleotide sequence data of parts of the 18S nrDNA, 28S nrDNA, ITS, GAPDH, RPB2 and TEF1-alpha gene regions. Our data reveal a Pleospora/Stemphylium clade sister to Embellisia annulata, and a well-supported Alternaria clade. The Alternaria clade contains 24 internal clades and six monotypic lineages, the assemblage of which we recognise as Alternaria. This puts the genera Allewia, Brachycladium, Chalastospora, Chmelia, Crivellia, Embellisia, Lewia, Nimbya, Sinomyces, Teretispora, Ulocladium, Undifilum and Ybotromyces in synonymy with Alternaria. In this study, we treat the 24 internal clades in the Alternaria complex as sections, which is a continuation of a recent proposal for the taxonomic treatment of lineages in Alternaria. Embellisia annulata is synonymised with Dendryphiella salina, and together with Dendryphiella arenariae, are placed in the new genus Paradendryphiella. The sexual genera Clathrospora and Comoclathris, which were previously associated with Alternaria, cluster within the Pleosporaceae, outside Alternaria s. str., whereas Alternariaster, a genus formerly seen as part of Alternaria, clusters within the Leptosphaeriaceae. Paradendryphiella is newly described, the generic circumscription of Alternaria is emended, and 32 new combinations and 10 new names are proposed. A further 10 names are resurrected, while descriptions are provided for 16 new Alternaria sections.

Taxonomic novelties: New combinations - Alternaria abundans (E.G. Simmons) Woudenb. & Crous, Alternaria alternariae (Cooke) Woudenb. & Crous, Alternaria atra (Preuss) Woudenb. & Crous, Alternaria bornmuelleri (Magnus) Woudenb. & Crous, Alternaria botrytis (Preuss) Woudenb. & Crous, Alternaria caespitosa (de Hoog & C. Rubio) Woudenb. & Crous, Alternaria cantlous (Yong Wang bis & X.G. Zhang) Woudenb. & Crous, Alternaria caricis (E.G. Simmons) Woudenb. & Crous, Alternaria cinerea (Baucom & Creamer) Woudenb. & Crous, Alternaria didymospora (Munt.-Cvetk.) Woudenb. & Crous, Alternaria fulva (Baucom & Creamer) Woudenb. & Crous, Alternaria hyacinthi (de Hoog & P.J. Mull. bis) Woudenb. & Crous, Alternaria indefessa (E.G. Simmons) Woudenberg & Crous, Alternaria leptinellae (E.G. Simmons & C.F. Hill) Woudenb. & Crous, Alternaria lolii (E.G. Simmons & C.F. Hill) Woudenb. & Crous, Alternaria multiformis (E.G. Simmons) Woudenb. & Crous, Alternaria obclavata (Crous & U. Braun) Woudenb. & Crous, Alternaria obovoidea (E.G. Simmons) Woudenb. & Crous, Alternaria oudemansii (E.G. Simmons) Woudenb. & Crous, Alternaria oxytropis (Q. Wang, Nagao & Kakish.) Woudenb. & Crous, Alternaria penicillata (Corda) Woudenb. & Crous, Alternaria planifunda (E.G. Simmons) Woudenb. & Crous, Alternaria proteae (E.G. Simmons) Woudenb. & Crous, Alternaria scirpinfestans (E.G. Simmons & D.A. Johnson) Woudenb. & Crous, Alternaria scirpivora (E.G. Simmons & D.A. Johnson) Woudenb. & Crous, Alternaria septospora (Preuss) Woudenb. & Crous, Alternaria slovaca (Svob.-Pol., L. Chmel & Bojan.) Woudenb. & Crous, Alternaria subcucurbitae (Yong Wang bis & X.G. Zhang) Woudenb. & Crous, Alternaria tellustris (E.G. Simmons) Woudenb. & Crous, Alternaria tumida (E.G. Simmons) Woudenb. & Crous, Paradendryphiella salina (G.K. Sutherl.) Woudenb. & Crous, Paradendryphiella arenariae (Nicot) Woudenb. & Crous. New names - Alternaria aspera Woudenb. & Crous, Alternaria botryospora Woudenb. & Crous, Alternaria brassicae-pekinensis Woudenb. & Crous, Alternaria breviramosa Woudenb. & Crous, Alternaria chlamydosporigena Woudenb. & Crous, Alternaria concatenata Woudenb. & Crous, Alternaria embellisia Woudenb. & Crous, Alternaria heterospora Woudenb. & Crous, Alternaria papavericola Woudenb. & Crous, Alternaria terricola Woudenb. & Crous. Resurrected names - Alternaria cetera E.G. Simmons, Alternaria chartarum Preuss, Alternaria consortialis (Thüm.) J.W. Groves & S. Hughes, Alternaria cucurbitae Letendre & Roum., Alternaria dennisii M.B. Ellis, Alternaria eureka E.G. Simmons, Alternaria gomphrenae Togashi, Alternaria malorum (Ruehle) U. Braun, Crous & Dugan, Alternaria phragmospora Emden, Alternaria scirpicola (Fuckel) Sivan. New sections, all in Alternaria - sect. Chalastospora Woudenb. & Crous, sect. Cheiranthus Woudenb. & Crous, sect. Crivellia Woudenb. & Crous, sect. Dianthicola Woudenb. & Crous, sect. Embellisia Woudenb. & Crous, sect. Embellisioides Woudenb. & Crous, sect. Eureka Woudenb. & Crous, sect. Infectoriae Woudenb. & Crous, sect. Japonicae Woudenb. & Crous, sect. Nimbya Woudenb. & Crous, sect. Phragmosporae Woudenb. & Crous, sect. Pseudoulocladium Woudenb. & Crous, sect. Teretispora Woudenb. & Crous, sect. Ulocladioides Woudenb. & Crous, sect. Ulocladium Woudenb. & Crous, sect. Undifilum Woudenb. & Crous. New genus - Paradendryphiella Woudenb. & Crous.

Keywords: Allewia; Chalastospora; Crivellia; Embellisia; Lewia; Nimbya; Paradendryphiella; Sinomyces; Teretispora; Ulocladium; Undifilum; systematics.

Fig. 1.

Bayesian 50 % majority rule consensus tree based on the GAPDH, RPB2 and TEF1 sequences of 121 strains representing the Alternaria complex. The Bayesian posterior probabilities (PP) and RAxML bootstrap support values (ML) are given at the nodes (PP/ML). Thickened lines indicate a PP of 1.0 and ML of 100. The tree was rooted to Stemphylium herbarum (CBS 191.86). The monotypic lineages are indicated by black dots.

Fig. 2.

Bayesian 50 % majority rule consensus tree based on the SSU, LSU and RPB2 sequences of 74 strains representing the Pleosporineae. The Bayesian posterior probabilities (PP) and RAxML bootstrap support values (ML) are given at the nodes (PP/ML). Thickened lines indicate a PP of 1.0 and ML of 100. The tree was rooted to Julella avicenniae (BCC 18422).

Fig. 3.

Alternaria sect. Alternantherae: conidia and conidiophores. A-D. A. alternantherae. E-H. A. perpunctulata. Scale bars = 10 μm.

Fig. 4.

Alternaria sect. Alternata: conidia and conidiophores. A, N. A. daucifolii. B, L-M. A. arborescens. C, H-J. A. alternata. D, O. A. gaisen. E. A. limoniasperae. F, K. A. tenuissima. G, P. A. longipes. Scale bars = 10 μm.

Fig. 5.

Alternaria sect. Brassicicola: conidia and conidiophores. A, H. A. brassicicola. B, I, L-M. A. mimicola. C, G. A. solidaccana. D, J-K. A. conoidea. E-F. A. septorioides. Scale bars = 10 μm.

Fig. 6.

Alternaria sect. Chalastospora: conidia and conidiophores. A. A. cetera. B. A. obclavata. C. A. breviramosa. D, H. A. armoraciae. E-G. A. abundans. Scale bars = 10 μm.

Fig. 7.

Alternaria sect. Cheiranthus: conidia and conidiophores. A-B. A. indefessa. B-C. A. cheiranthi. Scale bars = 10 μm.

Fig. 8.

Alternaria sect. Crivellia: conidia and conidiophores. A-B. A. papavericola. C-D. A. penicillata. Scale bars = 10 μm.

Fig. 9.

Alternaria sect. Dianthicola: conidia and conidiophores. A-B. A. dianthicola. C-E. A. simsimi. F-H. A. elegans. Scale bars = 10 μm.

Fig. 10.

Alternaria sect. Embellisia: conidia and conidiophores. A-D. A. embellisia. E-H. A. tellustris. Scale bars = 10 μm.

Fig. 11.

Alternaria sect. Embellisioides: conidia and conidiophores. A-B. A. hyacinthi. C-E. A. lolii. F-H. A. botryospora. I-K. A. planifunda. L-N. A. proteae. O-P. A. tumida. Scale bars = 10 μm.

Fig. 12.

Alternaria sect. Eureka: conidia and conidiophores. A-B. A. anigozanthi. C-D. A. cumini. E-F. A. leptinellae. G-H. A. triglochinicola. I-J. A. geniostomatis. K-L. A. eureka. Scale bars = 10 μm.

Fig. 13.

Alternaria sect. Gypsophilae: conidia and conidiophores. A-B. A. axiariisporifera. C-D. A. ellipsoidea. E-G. A. saponariae. H-I. A. vaccariae. J-K. A. nobilis. L-M. A. juxtiseptata. N-P. A. vaccariicola. Scale bars = 10 μm.

Fig. 14.

Alternaria sect. Infectoriae: conidia and conidiophores. A-B. A. ethzedia. C-D. A. infectoria. E-F. A. conjuncta. G-H. A. oregonensis. Scale bars = 10 μm.

Fig. 15.

Alternaria sect. Japonicae: conidia and conidiophores. A-B. A. japonica. C-E. A. nepalensis. Scale bars = 10 μm.

Fig. 16.

Alternaria sect. Nimbya: conidia and conidiophores. A-B. A. caricis. C-D. A. scirpicola. Scale bars = 10 μm.

Fig. 17.

Alternaria sect. Panax: conidia and conidiophores. A-B. A. avenicola. C-D. A. calycipyricola. E-F. A. panax. G-H. A. photistica. Scale bars = 10 μm.

Fig. 18.

Alternaria sect. Phragmosporae: conidia and conidiophores. A-B. A. didymospora. C. A. phragmospora. D-E. A. limaciformis. F-G. A. molesta. H-I. A. mouchaccae. Scale bars = 10 μm.

Fig. 19.

Alternaria sect. Porri: conidia and conidiophores. A-C. A. daucii. D-F. A. pseudorostrata. G-H. A. solani. Scale bars = 10 μm.

Fig. 20.

Alternaria sect. Pseudoulocladium: conidia and conidiophores. A-B. A. aspera. C-D. A. concatenata. E-F. A. chartarum. G-H. A. septospora. Scale bars = 10 μm.

Fig. 21.

Alternaria sect. Radicina: conidia and conidiophores. A-C. A. carotiincultae. D-E. A. petroselini. F-G. A. radicina. H-I. A. selini. J-L. A. smyrnii. Scale bars = 10 μm.

Fig. 22.

Alternaria sect. Sonchi: conidia and conidiophores. A-B. A. cinerariae. C-D. A. sonchi. Scale bars = 10 μm.

Fig. 23.

Alternaria sect. Teretispora: conidia and conidiophores. A-D. A. leucanthemi. Scale bars = 10 μm.

Fig. 24.

Alternaria sect. Ulocladioides: conidia and conidiophores. A-B. A. atra. C-D. A. brassicae-pekinensis. E-F. A. cantlous. G-H. A. multiformis. I-J. A. obovoidea. K-L. A. heterospora. M-N. A. subcucurbitae. O-P. A. terricola. Scale bars = 10 μm.

Fig. 25.

Alternaria sect. Ulocladium: conidia and conidiophores. A-B. A. capsici-annui. C-D. A. oudemansii. E-F. A. alternariae. G-H. A. botrytis. Scale bars = 10 μm.

Fig. 26.

Alternaria sect. Undifilum: conidia and conidiophores. A-D. A. bornmuelleri. Scale bars = 10 μm.

Fig. 27.

Paradendryphiella gen. nov.: conidia and conidiophores. A-B, D-E, G-I. P. salina. C, F. P. arenariae. Scale bars = 10 μm.