Stagonosporopsis

Stagonosporopsis Died. emend. Aveskamp et al., Stud. Mycol. 65: 44. 2010

Stagonosporopsis is a coelomycetous genus in the family Didymellaceae (de Gruyter et al. 2013), accommodating several important phytopathogenic species. Some of the species have described sexual forms in Didymella (Diedicke 1912; Aveskamp et al. 2010). Some Stagonosporopsis species have quarantine importance. Stagonosporopsis andigena is listed in Annex IAI by European Union (EU), meaning its introduction to EU is prohibited. This pathogen is also listed in the A1 list by the European and Mediterranean Plant Protection Organization (EPPO, 2019). Stagonosporopsis chrysanthemi is another species listed in A2 list by EPPO (EPPO, 2019).

Classification Dothideomycetes, Pleosporomycetidae, Pleosporales, Didymellaceae

Type speciesStagonosporopsis boltshauseri (Sacc.) Died. 1912

Distribution – Worldwide

Disease symptoms – the Black blight of potato, gummy stem blight, ray blight

All plant parts may be attacked by S. chrysanthemi and S. inoxydabilis, however, flowers and cuttings are highly susceptible. Death of flowers and buds, a necrotic lesion on leaves and peduncles of unopened buds, soft rot of cortex of roots and discolouration of bark are the main symptom of the disease. Eventually, plant death occurs (Fox 1998; Pethybridge et al. 2008). In gummy stem blight of cucurbits, symptoms can be observed on all above ground and reproductive parts. Leaf spots are the main diagnostic character of this disease. Most of the circular or triangular shaped spots start at the margin of the leaf or extend towards the margin. The centre of the leaf spot is a lighter shade of brown than the surrounding portion. As leaf spots coalesce leaf blights occur. Actively expanding lesions on leaves, petioles, and pedicels often appear as water-soaked. Cankers may form on crowns, main stems and vines (Keinath 2013). Stagonosporopsis andigena the black blight of potato causal agent affects leaves, petioles and stems causing lesions and premature leaf drop, but does not infect the underground parts. On leaves, the pathogen causes small, blackish concentric lesions. The initial symptoms can be observed on the lower leaves, however, as the disease progresses lesions may also develop in upper leaves as well. Lesions may coalesce and severely affected leaves may turn blackish giving a scorched appearance (French 2001; EFSA panel on plant health 2019).

HostsAmaranthaceae, Asteraceae, Campanulaceae, Caryophyllaceae, Cucurbitaceae, Fabaceae, Lamiaceae, Pinaceae, Ranunculaceae, Solanaceae and Valerianaceae.

 

Morphological based identification and diversity

Stagonosporopsis is characterized by ellipsoidal to subglobose, aseptate to 3 septate conidia and sexual morph with ellipsoidal, fusiform or obovoid, 1 septate ascospore (Aveskamp et al. 2010; Chen et al. 2015). Stagonosporopsis was originally separated from Ascochyta by Diedicke (1912) based on the occasional formation of multi-septate (Stagonospora-like) conidia. In the phylogenetic reassessment of Didymellaceae (Aveskamp et al. 2010) based on the sequences LSU and ITS of the nrDNA and TUB2 region, multiple Phoma species, including P. ligulicola, were recovered in a high supported clade with the interpretive types of the genus Stagonosporopsis; S. actaeae (Boerema et al. 1997, 2004). In addition, S. tanaceti shows morphological similarity to S. inoxydabilis but can be differentiated by the faster growth rate, larger conidia, presence of chlamydospores, and lack of ascomata in culture (Vaghefi et al. 2012). Morphological characters overlap between the species in this genus and species are primarily separated based on molecular data.

 

Molecular based identification and diversity

Most comprehensive multigene phylogeny analyses for this genus were performed by Aveskamp et al. (2010), Vaghefi et al. (2012), Hyde et al. (2014), Chen et al. (2015, 2017) and Jayasiri et al. (2019). Five-marker phylogeny of the Stagonosporopsis spp. for which these DNA sequence data are available is shown (Table ).

            Identification of Stagonosporopsis species associated with ray blight of Asteraceae can be achieved through multi-locus sequence typing (Aveskamp et al. 2010; Vaghefi et al. 2012) and also with a species-specific multiplex PCR assay developed by Vaghefi et al. (2016). This assay is based on a four-primer PCR that targets the intergenic spacer of the nrDNA of the ray blight pathogens, producing species-specific amplicons of ~ 560 in S. chrysanthemi, ~ 630 bp in S. inoxydabilis and ~ 400 bp in S. tanaceti, which can be easily differentiated on an agarose gel (Vaghefi et al. 2016).

This study reconstructs the phylogeny of Stagonosporopsis based on analyses of a combined ITS, LSU, RPB2 and TUB2 sequence data (Fig ). The phylogenetic tree is updated with recently introduced Stagonosporopsis species and corresponds to previous studies (Chen et al. 2017, Jayasiri et al. 2019).

 

Recommended genetic markers (genus level) – ITS

Recommended genetic markers (species level) – TUB2 and RPB2

Accepted number of species: There are 55 species in Index Fungorum (2019) and only 24 species are accepted/ have molecular data in this genus.

References: Chen et al. 2015, 2017, Jayasiri et al. 2019 (morphology, phylogeny).

 

Table Details of the Stagonosporopsis isolates used in the phylogenetic analyses. Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher stains are in bold.

Species Culture GenBank Accession numbers
    LSU ITS RPB2 TUB2
Stagonosporopsis actaeae CBS 106.96* GU238166 GU237734 KT389672 GU237671
CBS 114303 KT389760 KT389544 KT389847
S. ailanthicola MFLUCC 16-1439* KY100874 KY100872 KY100876 KY100878
S. ajacis CBS 177.93* GU238168 GU237791 KT389673 GU237673
S. andigena CBS 269.80 GU238170 GU237817 GU237675
CBS 101.80 GU238169 GU237714 GU237674
S. artemisiicola CBS 102636 GU238171 GU237728 KT389674 GU237676
S. astragali CBS 178.25 GU238172 GU237792 GU237677
S. caricae CBS 248.90 GU238175 GU237807 GU237680
CBS 282.76 GU238177 GU237821 GU237682
S. chrysanthemi CBS 500.63 GU238190 GU237871 GU237695
CBS 137.96 GU238191 GU237783 GU237696
S. crystalliniformis CBS 713.85* GU238178 GU237903 KT389675 GU237683
S. cucurbitacearum CBS 133.96 GU238181 GU237780 KT389676 GU237686
S. dennisii CBS 631.68* GU238182 GU237899 KT389677 GU237687
S. dorenboschii CBS 426.90* GU238185 GU237862 KT389678 GU237690
S. helianthi CBS 200.87* KT389761 KT389545 KT389683 KT389848
S. heliopsidis CBS 109182 GU238186 GU237747 KT389679 GU237691
S. hortensis CBS 104.42 GU238198 GU237730 KT389680 GU237703
CBS 572.85 GU238199 GU237893 KT389681 GU237704
S. inoxydabilis CBS 425.90* GU238188 GU237861 KT389682 GU237693
S. loticola CBS 562.81* GU238192 GU237890 KT389684 GU237697
S. lupini CBS 101494* GU238194 GU237724 KT389685 GU237699
S. oculo hominis CBS 634.92* GU238196 GU237901 KT389686 GU237701
S. pini MFLUCC 18-1549* MK348019 MK347800 MK434860
S. rudbeckiae CBS 109180 GU238197 GU237745 GU237702
S. tanaceti CBS 131484* JQ897461 NR_111724- JQ897496
S. trachelii CBS 379.71 GU238173 GU237850 KT389687 GU237678
CBS 384.68 GU238174 GU237856 GU237679
S. valerianellae CBS 273.92 GU238200 GU237819 GU237705
CBS 329.67* GU238201 GU237832 GU237706

Fig Phylogenetic tree generated by maximum likelihood analysis of combined ITS, LSU, RPB2 and TUB2 sequence data of Stagonosporopsis species. Related sequences were obtained from GenBank. Thirty-two are included in the analyses, which comprise 2756 characters including gaps. Single gene analyses were carried out and compared with each species, to compare the topology of the tree and clade stability. The tree was rooted with Heterophoma poolensis (CBS 113.20). Tree topology of the ML analysis was similar to the MP. The best scoring RAxML tree with a final likelihood value of -8386.622374 is presented. The matrix had 388 distinct alignment patterns, with 11.83% of undetermined characters or gaps. Estimated base frequencies were as follows; A = 0.245798, C = 0.237676, G = 0.273178, T = 0.243348; substitution rates AC = 1.882600, AG = 4.123164, AT = 2.015920, CG = 0.907833, CT = 12.626910, GT = 1.000000; gamma distribution shape parameter α = 1.105097. RAxML bootstrap support values ≥50% and Bayesian posterior probabilities ≥0.95 (BYPP) are shown respectively near the nodes. Ex-type strains are in bold.

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