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Restyling Alternaria Joyce H.C. Woudenberg Thesis committee Promotors Prof. Dr P.W. Crous Professor of Evolutionary Phytopathology Wageningen University Prof. Dr P.J.G.M. de Wit Professor of Phytopathology Wageningen University Co-promotor Dr J.Z. Groenewald Researcher, Evolutionary Phytopathology CBS-KNAW Fungal Biodiversity Centre, Utrecht Other members Dr F.T. Bakker, Wageningen University Dr A.J.M. Debets, Wageningen University Prof. Dr Th.W. Kuyper, Wageningen University Dr J. Woodhall, Food and Environment Research Agency (Fera), UK This research was conducted under the auspices of the Graduate School of Experimental Plant Sciences Restyling Alternaria Joyce H.C. Woudenberg Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Thursday 10 September 2015 at 11 a.m. in the Aula. Joyce H.C. Woudenberg Restyling Alternaria, 251 pages. PhD thesis, Wageningen University, Wageningen, NL (2015) With references, with summary in English ISBN 978-94-6257-410-6 CONTENTS Chapter 1 General introduction 7 Chapter 2 Alternaria redefined 19 Chapter 3 Reappraisal of the genus Alternariaster (Dothideomycetes) 79 Chapter 4 Large-spored Alternaria pathogens in section Porri 95 disentangled Chapter 5 Alternaria section Alternaria: species, formae speciales or 161 pathotypes Chapter 6 Diversity and movement of indoor Alternaria alternata 197 across the mainland USA Chapter 7 General discussion 219 Appendix References 230 Summary 243 Acknowledgements 246 Curriculum vitae 248 List of publications 249 Education statement 251 CHAPTER General introduction 1 Chapter 1 GENERAL INTRODUCTION The fungal genus Alternaria is an omnipresent dematiaceous hyphomycete which forms dark- coloured, multicellular conidia (phaeodictyospores). It includes saprophytic, endophytic and pathogenic species, and is associated with a wide variety of substrates including seeds, plants, agricultural products, humans, soil and the atmosphere. The pathogenic species include multiple serious plant pathogens, causing major losses on a wide range of crops (Thomma 2003), while others are again known as important post-harvest pathogens (Serdani et al. 2002, Kang et al. 2002), or causative agents of phaeohyphomycosis in immuno-compromised patients (Pastor & Guarro 2008). When occurring indoors, they are also common allergens in humans causing hypersensitivity reactions, which can eventually lead to asthma (Downs et al. 2001). Molecular studies reveal that the Alternaria complex currently comprises the genera Alternaria, Chalastospora, Crivellia, Embellisia, Nimbya, Stemphylium, Ulocladium, Undifilum and the recently described genus Sinomyces (Fig. 1). Several genera within this complex are non-monophyletic and Alternaria species cluster in multiple distinct species- clades, which are not always correlated with species-groups based upon morphological characteristics. Alternaria alternata, the most commonly reported species in literature and type species of the genus Alternaria, also comprises one such a species-group (Simmons 1995). These small-spored Alternaria species can, however, not be distinguished based on molecular techniques alone (Peever et al. 2004, 2005, Andrew et al. 2009). As A. alternata is considered as one of the most prolific producers of fungal allergens (Horner et al. 1995, Pulimood et al. 2007, Kuna et al. 2011), and this species complex contains multiple host- specific pathogenic strains (Kohmoto & Otani 1991), a correct identification is of utmost importance. Taxonomic history The genus Alternaria was first described withA. tenuis as the type, and only species (Nees 1816). The characteristics of the genus included the production of dark-coloured dictyospores in chains, and a beak of tapering apical cells. The genus was initially not recognized and A. tenuis was erroneous synonymised with Torula alternata (Fries 1832), and multiple new phaeodictyosporic hyphomycetous genera were described, such as Macrosporium (Fries 1832), Stemphylium (Wallroth 1833) and Ulocladium (Preuss 1851), further complicating the taxonomic resolution in this group of fungi. Several re-descriptions of these genera (Saccardo 1886, Elliot 1917) resulted in a growing number of new species. Due to ambiguities in the description of A. tenuis (Nees 1816), both A. tenuis and T. alternata were later synonymised under Alternaria alternata (Keissler 1912), and Macrosporium was synonymised under Alternaria after re-examination of their respective type species (Wiltshire 1933). Furthermore, the genus concept of Stemphylium was re-defined (Wiltshire 1938) and a later review of the genus Alternaria and related species (Joly 1964) placed a lot of atypical strains back into Alternaria. Fig. 1. Bayesian 50 % majority rule consensus tree based on GAPDH sequence data from Pryor & Bigelow (2003), Hong et al. (2005), Andersen et al. (2009), Pryor et al. (2009), Runa et al. (2009), Lawrence et al. (2011), and Wang et al. (2011). The Bayesian posterior probabilities (PP) > 0.75 are presented at the nodes; thickened lines indicate a PP of 1.0. The blue boxes indicate the Alternaria species-groups. The tree was rooted with Setosphaeria pedicellata. 8 General introduction AY562408 A. capsici 1 GAPDH locus AY278804 A. crassa AY562405 A. blumeae 114 isolates, 474 characters 0.97 AY278805 A. macrospora AY562409 A. cucumerina GTR + γ distribution model AY562406 A. pseudorostrata 207 unique site patterns AY562417 A. euphorbiicola AY278803 A. dauci AY562407 A. tagetica 0.82 AY278807 A. solani AY278806 A. porri AY562410 A. dumosa AY278811 A. longipes AY278808 A. alternata AY278812 A. destruens AY278810 A. arborescens AY278809 A. tenuissima 0.92 AY562411 A. limoniasperae JN383477 A. alternantherae Alternaria I JN383479 A. perpunctulata JN383478 A. celosiae 0.90 AY278797 A. radicina FJ266496 U. lanuginosum AY278798 A. carotiincultae AY278799 A. petroselini AY278800 A. selini AY278801 A. smyrnii AY562412 A. sonchi AY562413 A. cinerariae 0.76 AY562414 A. brassicae AY562415 A. mimicula AY278813 A. brassicicola FJ348227 E. conoidea 0.99 FJ214854 A. photistica AY562416 A. eryngii AY278814 A. japonica 0.94 FJ266501 U. tuberculatum 0.91 AY278818 U. atrum 0.96 AY562418 U. cucurbitae 0.92 AY278817 U. botrytis FJ266495 U. dauci 0.86 FJ266498 U. obovoideum FJ266497 U. multiforme Ulocladium AY278816 U. consortiale FJ266494 U. consortiale AY278802 A. cheiranthi AY278828 E. indefessa 0.95 AY278819 U. chartarum FJ266500 U. septosporum JN383469 E. dennisii FJ357306 U. oxytropis FJ357308 U. oxytropis Undifilum FJ357305 U. bornmuelleri FJ214834 A. triticimaculans AY278796 A. triticina FJ214855 A. ethzedia AY278795 A. ethzedia FJ214849 A. oregonensis AY562403 A. oregonensis 0.95 FJ214835 A. metachromatica AY562401 A. conjuncta AY562404 A. metachromatica Alternaria II FJ214850 A. infectoria AY278793 A. infectoria FJ214831 A. intercepta 0.88 FJ214825 A. viburni AY562402 A. photistica 0.99 FJ214806 A. arbusti FJ214846 A. triticina FJ214813 C. cetera 0.91 AY562398 C. cetera FJ214851 E. abundans FJ214852 E. abundans Chalastospora FJ214809 C. gossypii FJ214810 C. gossypii JN383474 E. phragmospora 0.90 FJ357302 E. phragmospora AY562399 A. mouchaccae Embellisia I JN383470 E. didymospora FJ357300 E. didymospora 0.91 0.98 AY562419 E. telluster 0.88 FJ357304 E. telluster 0.98 JN383468 E. chlamydospora Embellisia II AY278827 E. allii JN383480 N. scirpinfestans JN383481 N. scirpivora Nimbya AY278825 N. scirpicola AY278826 N. caricis FJ357298 Brachycladium papaveris HM209083 Crivellia papaveracea Crivellia 0.90 FJ357299 Crivellia papaveracea HM209081 S. fusoideus HM209082 S. fusoideus AY278815 S. alternariae Sinomyces FJ266499 U. oudemansii AY562400 A. argyranthemi JN383476 E. thlaspi FJ357303 E. planifunda FJ266493 E. tumida 0.99 0.99 FJ266492 E. planifunda AY278830 E. hyacinthi 0.99 AY278831 E. novae-zelandiae Embellisia III 0.99 AY278829 E. proteae JN383473 E. lolii FJ357301 E. lolii JN383472 E. leptinellae 0.94 AY278832 E. leptinellae Embellisia IV JN383471 E. eureka AY278821 S. vesicarium 0.94 AY278823 P. herbarum AY278822 S. callistephi Stemphylium AY278820 S. botryosum JN383467 E. annulata AY278824 Setosphaeria pedicellata 0.1 9 Chapter 1 The current concepts of the genera started with the seminal paper “Typification of Alternaria, Stemphylium and Ulocladium” (Simmons 1967) followed by multiple Alternaria essays, where two additional asexual genera were described as close relatives of Alternaria, namely Embellisia (Simmons 1971) and Nimbya (Simmons 1989). A life-time work on Alternaria taxonomy eventually resulted in The Alternaria Identification Manual (Simmons 2007), with morphological descriptions of 275 recognised Alternaria species. Here again three new genera, Alternariaster, Chalastospora, and Teretispora, were segregated from Alternaria, based on morphological characters. Meanwhile, the sexual genus Crivellia with Brachycladium as asexual morph was described (Inderbitzin et al. 2006), to accommodate a former Pleospora species. Based on morphological and molecular data Crivellia was shown to belong to the Alternaria complex rather than to Pleospora. The genus Undifilum was described to accommodate two species formerly classified in Embellisia and Helminthosporium (Pryor et al. 2009). Based on molecular data Undifilum formed a distinct clade from the other Embellisia species and species in Alternaria, Ulocladium, Nimbya and Crivellia.
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  • Reappraisal of the Genus Alternariaster (Dothideomycetes)

    Reappraisal of the Genus Alternariaster (Dothideomycetes)

    Persoonia 31, 2013: 77–85 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE http://dx.doi.org/10.3767/003158513X669030 Reappraisal of the genus Alternariaster (Dothideomycetes) J.L. Alves1, J.H.C. Woudenberg2, L.L. Duarte1, P.W. Crous2,3,4, R.W. Barreto1 Key words Abstract Alternariaster was erected in 2007 to accommodate Alternaria helianthi, a fungal species known to cause leaf spots on Helianthus annuus (sunflower). It was segregated from Alternaria based on conidial morphol- Alternaria ogy. Recently an unknown alternaria-like dematiaceous fungus was found associated with leaf spots on Bidens fungal pathogens sulphurea (yellow cosmos) in Brazil. Based on a multi-gene phylogeny of parts of the ITS and LSU genes, this host-range fungus was placed within the Leptosphaeriaceae with Alternariaster helianthi as its closest neighbour. Additional multi-gene phylogeny genes sequenced, RPB2 and GAPDH, confirmed this close relationship. The fungus on B. sulphurea has smaller conidia, 50–97.5 × 12.5–20 µm, compared to Al. helianthi, 80–160 × 18–30 µm, and lacks oblique or transverse septa which can be present in Al. helianthi. Pathogenicity studies on 18 plant species belonging to the Compositae showed that the B. sulphurea fungus only infected B. sulphurea, whereas Al. helianthi infected H. annuus and Ga- linsoga quadriradiata, a yet unreported host of Al. helianthi. The fungus causing disease on B. sulphurea is hence closely related but phylogenetically, morphologically and pathologically distinct from Al. helianthi, and therefore newly described as Alternariaster bidentis. The collection of a second species in the genus Alternariaster and the multigene phylogenetic analysis of these two species, confirmed Alternariaster to be a well-delimited genus in the Leptosphaeriaceae rather than the Pleosporaceae, to which Alternaria belongs.