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. 2013 Jun 30;75(1):213-305.
doi: 10.3114/sim0018.

A new approach to species delimitation in Septoria

G J M Verkley  1 , W Quaedvlieg, H-D Shin, P W Crous
Affiliations

A new approach to species delimitation in Septoria

G J M Verkley et al. Stud Mycol. .

Abstract

Septoria is a large genus of asexual morphs of Ascomycota causing leaf spot diseases of many cultivated and wild plants. Host specificity has long been a decisive criterium in species delimitation in Septoria, mainly because of the paucity of useful morphological characters and the high level of variation therein. This study aimed at improving the species delimitation of Septoria by adopting a polyphasic approach, including multilocus DNA sequencing and morphological analyses on the natural substrate and in culture. To this end 365 cultures preserved in CBS, Utrecht, The Netherlands, among which many new isolates obtained from fresh field specimens were sequenced. Herbarium material including many types was also studied. Full descriptions of the morphology in planta and in vitro are provided for 57 species. DNA sequences were generated for seven loci, viz. nuclear ITS and (partial) LSU ribosomal RNA genes, RPB2, actin, calmodulin, Btub, and EF. The robust phylogeny inferred showed that the septoria-like fungi are distributed over three main clades, establishing the genera Septoria s. str., Sphaerulina, and Caryophylloseptoria gen. nov. Nine new combinations and one species, Sphaerulina tirolensis sp. nov. were proposed. It is demonstrated that some species have wider host ranges than expected, including hosts from more than one family. Septoria protearum, previously only associated with Proteaceae was found to be also associated with host plants from six additional families of phanerogams and cryptogams. To our knowledge this is the first study to provide DNA-based evidence that multiple family-associations occur for a single species in Septoria. The distribution of host families over the phylogenetic tree showed a highly dispersed pattern for 10 host plant families, providing new insight into the evolution of these fungi. It is concluded that trans-family host jumping is a major force driving the evolution of Septoria and Sphaerulina.

Taxonomic novelties: New genus - Caryophylloseptoria Verkley, Quaedvlieg & Crous; New species - Sphaerulina tirolensis Verkley, Quaedvlieg & Crous; New combinations - Caryophylloseptoria lychnidis (Desm.) Verkley, Quaedvlieg & Crous, Caryophylloseptoria silenes (Westend.) Verkley, Quaedvlieg & Crous, Caryophylloseptoria spergulae (Westend.) Verkley, Quaedvlieg & Crous, Sphaerulina aceris (Lib.) Verkley, Quaedvlieg & Crous, Sphaerulina cornicola (DC.: Fr.) Verkley, Quaedvlieg & Crous, Sphaerulina gei (Roberge ex Desm.) Verkley, Quaedvlieg & Crous, Sphaerulina hyperici (Roberge ex Desm.) Verkley, Quaedvlieg & Crous, Sphaerulina frondicola (Fr.) Verkley, Quaedvlieg & Crous, Sphaerulina socia (Pass.) Quaedvlieg, Verkley & Crous; Epitypifications (basionyms) - Ascochyta lysimachiae Lib., Septoria astragali Roberge ex Desm., Septoria cerastii Roberge ex Desm., Septoria clematidis Roberge ex Desm., Septoria cruciatae Roberge ex Desm., Septoria spergulae Westend., Septoria epilobii Westend., Septoria galeopsidis Westend., Septoria gei Roberge ex Desm., Septoria hyperici Roberge ex Desm., Septoria rubi Westend., Septoria senecionis Westend., Septoria urticae Roberge ex Desm.

Keywords: Evolution; Multilocus Sequence Typing (MLST); Mycosphaerella; Mycosphaerellaceae; Phloeospora; Pleosporales; Septoria; Sphaerulina; host jumping; host specificity; new genus; new species; systematics; taxonomy.

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Figures

Fig. 1.
Fig. 1.
Frequency distributions of the Kimura-2-parameter distances (barcoding gaps) for the seven PCR loci.
Fig. 2.
Fig. 2.
Consensus phylogram (50 % majority rule) of 17 222 trees resulting from a Bayesian analysis of the combined seven loci sequence alignment using MrBayes v. 3.2.1. Bayesian posterior probabilities values are indicated on their respective branches and the scale bar indicates 0.2 expected changes per site. The tree was rooted to Readeriella mirabilis (Teratosphaeriaceae) (CBS 125000). The family of the host plant from which the strain was isolated is indicated for 12 most prevalently occurring host families in our dataset (colour bar according to the legend).
Fig. 2.
Fig. 2.
Consensus phylogram (50 % majority rule) of 17 222 trees resulting from a Bayesian analysis of the combined seven loci sequence alignment using MrBayes v. 3.2.1. Bayesian posterior probabilities values are indicated on their respective branches and the scale bar indicates 0.2 expected changes per site. The tree was rooted to Readeriella mirabilis (Teratosphaeriaceae) (CBS 125000). The family of the host plant from which the strain was isolated is indicated for 12 most prevalently occurring host families in our dataset (colour bar according to the legend).
Fig. 2.
Fig. 2.
Consensus phylogram (50 % majority rule) of 17 222 trees resulting from a Bayesian analysis of the combined seven loci sequence alignment using MrBayes v. 3.2.1. Bayesian posterior probabilities values are indicated on their respective branches and the scale bar indicates 0.2 expected changes per site. The tree was rooted to Readeriella mirabilis (Teratosphaeriaceae) (CBS 125000). The family of the host plant from which the strain was isolated is indicated for 12 most prevalently occurring host families in our dataset (colour bar according to the legend).
Fig. 3.
Fig. 3.
Caryophylloseptoria lychnidis. A. CBS 109098, colony on OA. B. Ibid., on CMA. C. Conidia and conidiogenous cells in planta (CBS 109098). D. Conidia on OA (CBS 109098). Scale bars = 10 μm.
Fig. 4.
Fig. 4.
Caryophylloseptoria silenes. A-C. Colonies CBS 109100. A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells in planta (CBS H-21160). E. Ibid., on OA (CBS 109100). F-G. Conidia on OA (CBS 109100). Scale bars = 10 μm.
Fig. 5.
Fig. 5.
Caryophylloseptoria spergulae. A, B. Colonies CBS 109010. A. On OA. B. On MEA. C. Conidia and conidiogenous cells in planta (CBS H-21150). D-H. Conidia on OA (CBS 109010). Scale bars = 10 μm.
Fig. 6.
Fig. 6.
Septoria aegopodii. A-E. Conidia in planta. A-C. CBS H-21262. D, E. CBS H-21199. Scale bars = 10 μm.
Fig. 7.
Fig. 7.
Septoria aegopodina. A, B. Colonies CBS 123740. A. On OA. B. On MEA. C-F. Conidia in planta (CBS H-21249). G. Conidia and conidiogenous cells in planta (CBS H-21249). H, I. Conidia on OA (CBS 123741). J. Conidia on MEA (CBS 123740). Scale bars = 10 μm.
Fig. 8.
Fig. 8.
Septoria anthrisci. A. Conidia and conidiogenous cells in planta (CBS H-21185). B. Conidia on OA (CBS 109020). Scale bars = 10 μm.
Fig. 9.
Fig. 9.
Septoria apiicola. a. Colony on OA (CBS 400.54). B, C. Conidia in planta (CBS H-21261). D. Conidia on OA (CBS 400.54). E. Conidia and conidiogenous cells on OA (CBS 400.54). F. Ibid., in planta (CBS H-21261). Scale bars = 10 μm.
Fig. 10.
Fig. 10.
Septoria astragali, CBS 109116. A-C. Colonies (15 C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells on OA (CBS 109116); E-G. Conidia in planta (CBS H-21258). H. Conidiogenous cells on OA (CBS 123878). I. Conidia on OA (CBS 123878). Scale bars = 10 μm.
Fig. 11.
Fig. 11.
Septoria campanulae. A. Conidia and conidiogenous cells in planta (CBS H-21178). B. Ibid., on CHA (CBS 109114). Scale bars = 10 μm.
Fig. 12.
Fig. 12.
Septoria cerastii, CBS 102323. A-C. Colonies (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells in planta (CBS H-21158, epitype). E. Conidia on OA (CBS 102323). Scale bars = 10 μm.
Fig. 13.
Fig. 13.
Septoria clematidis. A, B. Colonies CBS 108983 (15 °C, nUV). A. On OA. B. On MEA. C. Conidia and conidiogenous cells in planta (CBS H-21182, epitype). D. Ibid., CBS 108983 on OA. Scale bars = 10 μm.
Fig. 14.
Fig. 14.
Septoria convolvuli. A, B. Conidia in planta (CBS H-21244). C. Conidia and conidiogenous cells on OA (CBS 102325). Scale bars = 10 μm.
Fig. 15.
Fig. 15.
Septoria cruciatae. A, B. Colonies CBS 123747. A. On OA. B. On MEA. C, D. Conidia in planta (CBS H-21250, epitype). E. Conidia on OA (CBS 123748). F. Conidia in planta (CBS H-21250). G. Conidia and conidiogenous cells in planta (CBS H-21250). H. Conidia on OA (CBS 123747). Scale bars = 10 μm.
Fig. 16.
Fig. 16.
Septoria cucubali. A-C. Colonies. A. CBS 102367, on OA. B. Ibid., on CHA. C, D. CBS 102386. C. On MEA. D. On OA. E, F. Conidia on OA (CBS 102386). G. Conidia and spermatia on OA (CBS 102367). H. Conidia and conidiogenous cells in planta (CBS H-21159). I. Conidia on OA (CBS 102386). Scale bars = 10 μm.
Fig. 17.
Fig. 17.
Septoria digitalis. A, B. Colonies CBS 328.67 (15 °C, nUV). A. On OA. B. On MEA. C, D. Colonies CBS 391.63 (15 °C, nUV). C. On OA. D. On MEA. E. Conidia on OA (CBS 328.67). Scale bars = 10 μm.
Fig. 18.
Fig. 18.
Septoria epilobii. A-C. Colonies CBS 109084 (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia in planta (CBS H-21171, epitype). E. Conidia and conidiogenous cells on OA (CBS 109094). Scale bars = 10 μm.
Fig. 19.
Fig. 19.
Septoria erigerontis. A-C. Colonies CBS 109094 (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia in planta (CBS H-21176). E. Conidia and conidiogenous cells on OA (CBS 109094). F, G. Conidia in planta (CBS H-21176). H, I. Conidia on OA (CBS 186.93). Scale bars = 10 μm.
Fig. 20.
Fig. 20.
Septoria galeopsidis, CBS 102314. A-C. Colonies (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia on OA. E. Conidia and conidiogenous cells in planta (CBS H-21195). F-H. Conidia on OA (CBS 123744). Scale bars = 10 μm.
Fig. 21.
Fig. 21.
Septoria heraclei, conidia and conidiogenous cells in planta (CBS H-21224). Scale bars = 10 μm.
Fig. 22.
Fig. 22.
Septoria hypochoeridis, CBS H-21234. A, B. Conidia in planta. Scale bars = 10 μm.
Fig. 23.
Fig. 23.
Septoria lactucae. A-D. Colonies CBS 108943 (15 °C, nUV). A. On OA. B. On MEA. C. Colony margin on OA. D. Colony margin on MEA. E-I. Conidia on OA (CBS 108943). Scale bars = 10 μm.
Fig. 24.
Fig. 24.
Septoria lamiicola, CBS 102329. A-C. Colonies (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia in planta (CBS H-21181). E. Ibid. (CBS H-21216). F. Conidia and conidiogenous cells on OA (CBS 102380). Scale bars = 10 μm.
Fig. 25.
Fig. 25.
Septoria leucanthemi. A-C. Colonies CBS 109090 (15 °C, nUV). A. On OA. B. On MEA. C. On CHA. D. Conidia and conidiogenous cells on OA (CBS 109090). E, F. Conidia in planta (CBS H-21243). G. Conidia on MEA (CBS 109090). Scale bars = 10 μm.
Fig. 26.
Fig. 26.
Septoria lycoctoni. A-C. Colonies CBS 109089 (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells in planta (CBS H-21155). E. Conidia on OA (CBS 109089). Scale bars = 10 μm.
Fig. 27.
Fig. 27.
Septoria lysimachiae. A-C. Colonies (15 °C, nUV). A. CBS 123794 on OA. B. CBS 108998 on MEA. C. Ibid., colony margin on MEA. D. Conidia in planta (CBS H-21196). E. Conidia on OA (CBS 108998). F. Conidia in planta (CBS H-21196). G. Conidia on OA (CBS 108998). H. Conidia on OA (CBS 108999). Scale bars = 10 μm.
Fig. 28.
Fig. 28.
Septoria matricariae. A. Conidia and conidiogenous cells in planta (CBS H-21228). B. Conidia on OA (CBS 109001). Scale bars = 10 μm.
Fig. 29.
Fig. 29.
Septoria melissae, CBS 109097. A-C. Colonies (15 °C, nUV). A. On OA. B. On MEA. C. On MEA, detail of colony margin. D. Conidia and conidiogenous cells on OA. E-F. Conidia on OA. Scale bars = 10 μm.
Fig. 30.
Fig. 30.
Septoria napelli. A-C. Colonies CBS 109104 (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells on OA (CBS 109104). E. Conidia in planta (CBS H-21153). Scale bars = 10 μm.
Fig. 31.
Fig. 31.
Septoria paridis. A-C. Colonies (15 °C, nUV). A. On OA (CBS 109110). B. On CHA (CBS 109110). C. On MEA (CBS 109108). D. Conidia and conidiogenous cells in planta (CBS H-21177, Paris quadrifolia). E. Ibid. (CBS H-21152, Viola palustris). F. Conidia on OA (CBS 109108). Scale bars = 10 μm.
Fig. 32.
Fig. 32.
Septoria petroselini. A, B. Colonies CBS 109521 (15 °C, nUV). A. On OA. B. On MEA. C, D. Conidia on OA (CBS 109521). E. Conidia and conidiogenous cells in planta (CBS H-21166). F. Conidia on OA (CBS 182.44). G. Conidia on OA (CBS 109521). Scale bars = 10 μm.
Fig. 33.
Fig. 33.
Septoria phlogis. Conidia and conidiogenous cells in planta (CBS H-21198). Scale bars = 10 μm.
Fig. 34.
Fig. 34.
Septoria polygonorum. A-C. Colonies CBS 102331 (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells in planta (CBS H-21212). E. Ibid., on OA (CBS 108982). F, G. Conidia on OA (CBS 347.67). Scale bars = 10 μm.
Fig. 35.
Fig. 35.
A-E. Septoria senecionis. A-C. Colonies CBS 102381 (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells in planta (CBS H-21219, epitype). E. Conidia in planta (CBS H-21219). F-J. Septoria putrida. F, G. Conidia in planta (CBS H-21174). H. Conidiogenous cells in planta (CBS H-21174). I. Conidia and conidiogenous cells in planta (CBS H-21174). J. Ibid., on OA (CBS 109088). Scale bars = 10 μm.
Fig. 36.
Fig. 36.
Septoria scabiosicola, CBS 102333. A-C. Colonies (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells in planta (CBS H-21180). E. Conidia on OA (CBS 109021). Scale bars = 10 μm.
Fig. 37.
Fig. 37.
Septoria sii. A-C. Colonies CBS 102370 (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells in planta (CBS H-21223). E. Ibid., on OA (CBS 102369). Scale bars = 10 μm.
Fig. 38.
Fig. 38.
Septoria sisyrinchii, CBS 112096. A-D. Colonies (15 °C, nUV). A. On OA. B. Ibid., reverse. C. On MEA. D. Ibid., detail of colony margin. E-G. Conidia on OA. Scale bars = 10 μm.
Fig. 39.
Fig. 39.
Septoria stachydis. A-C. Colonies CBS 102337 (15 °C, nUV). A. On OA. B. On CHA. C. On MEA. D. Conidia in planta (CBS H-21226). E. Conidia in planta (CBS H-21175). F-I. Conidia on OA (CBS 123750). Scale bars = 10 μm.
Fig. 40.
Fig. 40.
Septoria stellariae. A-D. Colonies CBS 102364. A, B. On OA. C. On CHA. D. On MEA. E. Conidia and conidiogenous cells on OA (CBS 102364). Scale bars = 10 μm.
Fig. 41.
Fig. 41.
Septoria urticae, epitype. A. Conidia and conidiogenous cells in planta (CBS H-21221). B. Ibid., on OA (CBS 102371). Scale bars = 10 μm.
Fig. 42.
Fig. 42.
Septoria verbenae. A. Conidia and conidiogenous cells in planta (CBS H-21241). B. Conidia on OA (CBS 113438). Scale bars = 10 μm.
Fig. 43.
Fig. 43.
Sphaerulina aceris. A, B. Colonies CBS 183.97. A. On OA. B. On MEA. C, D. Conidia in planta (CBS H-21239). Scale bars = 10 μm.
Fig. 44.
Fig. 44.
Sphaerulina cornicola. A-C. Colonies CBS 102324. A. On OA. B. On CHA. C. On MEA.
Fig. 45.
Fig. 45.
A-D. Sphaerulina hyperici. A-C. Colonies CBS 102313. A. On OA. B. On CHA. C. On MEA. D. Conidia and conidiogenous cells in planta (CBS H-21194, epitype). E-G. Sphaerulina gei. E. Colony on OA (KACC 44051 = CBS 128632). F. Conidia and conidiogenous cells in planta (CBS H-21194, epitype). G. Ibid., on OA (CBS 102318). Scale bars = 10 μm.
Fig. 46.
Fig. 46.
Sphaerulina tirolensis. A. Conidia in planta (CBS H-21232, holotype). B. Conidia on OA (CBS 109017). Scale bars = 10 μm.
Fig. 47.
Fig. 47.
Sphaerulina westendorpii. A. conidia in planta (CBS H-21229, epitype); B. conidia on OA (CBS 102327). Scale bars = 10 μm.
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