17 Sep Elsinoe

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Elsinoe Racib. [as ‘Elsinoë‘], Parasit. Alg. Pilze Java’s (Jakarta) 1: 14 (1900)

Background

Elsinoe was introduced by Raciborski (1900) based on E. canavaliae (Hyde et al. 2013; Jayawardena et al. 2014). von Arx & Müller (1975) placed this genus in Myriangiaceae based on the nature of its pseudoascostromata and parasitic nature. Later, the genus was placed in family Elsinoaceae (Barr 1979; Kirk et al. 2001; Lumbsch and Huhndorf 2007, 2010; Hyde et al. 2013; Jayawardena et al. 2014; Wijayawardene et al. 2017b). Elsinoe is characterized by forming scab-like lesions with pseudoascostromata containing three to eight bitunicate asci in each locule (Jayawardena et al. 2014).The asexual morph is the acervular coelomycetous Sphaceloma de Bary (Wijayawardene et al. 2012, 2017a). Jenkins (1932) proposed a connection between Sphaceloma and Elsinoe. As the sexual morph is not common in nature, morphological based identification of Elsinoe species is difficult. The asexual morph Sphaceloma frequently occurs in nature, however, its morphological characters overlap making identification of the species difficult. Examination of specimens collected in the field is also problematic due to the lack of fertile structures. Isolation of Elsinoë species is also challenging due to their slow growth (Jenkins 1932). In past, scab symptoms have been considered as a major character in recognizing the presence of fungi belonging to this genus, when sporulation is absent (Bitancourt and Jenkins 1949). Fan et al. (2017) suggested that even if spores are absent, species can be named if they have the support of successful isolations, resulting in cultures having common characteristics of the genus. The colonies of this genus are slow growing, raised, cerebriform or corrugated, dark red, orange or brown. If cultures cannot be obtained they should be considered as doubtful species until fertile specimens or pure cultures are obtained (Fan et al. 2017).

Many studies over the past decade have identified secondary metabolites of this genus (Hyde et al. 2013). Elsinochrome is a non-host selective, light-activated polyketide-derived toxin produced by Elsinoe species (Chung and Liao 2008). This is a red-pigmented secondary metabolite mainly produced by E. fawecettii (Yang and Chung 2010). Elsinopirini is a decalin polyketide isolated as a colourless oil from E. pyri (Surup et al. 2018). Production of these secondary metabolites can be used in chemotaxonomy.

 

Classification – Dothideomycetes, Dothideomycetidae, Myriangiales, Elsinoaceae

Type species – Elsinoe canavaliae Racib. [as ‘canavalliae’], Parasit. Alg. Pilze Java’s (Jakarta) 1: 14 (1900)

Distribution – Worldwide

Disease Symptoms – Scab, Anthracnose of grapevine

Many species cause scab like blemishes (Jayawardena et al. 2014). They can affect leaves, stems and fruits affecting the appearance as well as reducing the yield. Infected organs of some hosts (Cassava) develop severe distortions (Guatimosim et al. 2015).

Hosts – All members of this genus are specialized plant pathogens causing diseases on many economically important crops such as Citrus, Malus, Rubus and Vitis (Hyde et al. 2013; Jayawardena et al. 2014; Fan et al. 2017). The species appear to have a narrow host range, usually limited to a single host (Fan et al. 2017). However, a few species have a broad host range e.g., E. anacardii, E. leucospermi, E. piri and E. viola.

 

Morphological based identification and diversity

Kirk et al. (2008) estimated that there are 48 species of Elsinoe and 52 species of Sphaceloma. There are 190 species epithets under Elsinoe and 169 epithets under Sphaceloma in Index Fungorum (Index Fungorum 2018). Most Elsinoe species described to date need to be recollected and epitypified. Fan et al. (2017) designated 13 epitypes based on taxonomy and phylogenetic data. In accordance with the “One Fungus, one name” concept, the sexual name Elsinoe was protected over Sphaceloma. Therefore, many names in Sphaceloma should be transferred to the genus Elsinoe. Fan et al. (2017) relocated 26 Sphaceloma species to Elsinoe. In their study, eight new species were introduced, leading to a total of 75 Elsinoe species supported by morphology and molecular data.

Colony and spore morphology are the primary characters to identify species of Elsinoe (Fan et al. 2017). Species have overlapping colony and spore characters making identification based on morphology difficult. Therefore, use of DNA sequence data is crucial in identifying these species.

 

Molecular based identification and diversity

The first molecular study on this genus was by Tan et al. (1996), who investigated the genetic differences among the citrus scab pathogens E. fawcettii and E. australis from South America and S. fawcettii var. scabiosa from Australia. The asexual morph and sexual morph relationship was resolved by Cheewangkoon et al. (2009) by analysing rDNA sequence data. Few molecular studies have been carried out on this genus. Schoch et al. (2006) and Boehm (2009) using rDNA data showed that the species of Elsinoe constitute a subclade among the species of Myriangiaceae. However, Schoch et al. (2006) used only four Elsinoe strains and one Myrangium strain. Swart et al. (2001), based on ITS sequence data, delineated six Elsinoe species associated with the scab disease of Proteaceae and proposed three new species. Similar studies (e.g., Summerbell et al. 2006; Everett et al. 2011) described species of this genus associated with other host plants. Everett et al. (2011) and Hyde et al. (2013) carried out higher level phylogenetic studies on Dothideomycetes, which included strains of Elsinoe. Jayawardena et al. (2014) using the available sequence data on ITS, LSU, SSU, RPB2 and TEF1-α in GenBank provided evidence that Elsinoaceae can be considered as a separate family within the order Myriangiales. At the time, 12 Elsinoe species were included in this analysis, but ex-type sequence data was available for only a few species. Most species are based on old specimens without sequence data (Jayawardena et al. 2014). Fan et al. (2017) used 119 isolates representing 67 host genera from 17 countries and analysed a combined multigene analysis (ITS, LSU RPB2 and TEF1-α) with 64 ex-type strains. However, Jayawardena et al. (2014) and Fan et al. (2017) were unable to include the generic type E. canavaliae due to a lack of DNA data. Even though there are several excellent studies on this genus associated with plant diseases, very few species have any available cultures or DNA data (Jenkins 1932 a, b, Bitancourt and Jenkins 1936). Therefore, epitypification from fresh collections is required to provide a stable and a workable taxonomy for this genus. This study reconstructs the phylogeny of Elsinoe based on a combined ITS, LSU, RPB2 and TEF1-α sequence data, updated with recently introduced species and it corresponds with previous studies.

 

Recommended genetic markers (Genus level) – ITS

Recommended genetic markers (Species level) – RPB2, TEF-1

Accepted number of species: There are more than 200 species epithets in Index Fungorum (2018) under this genus. However, only 75 species have molecular data are treated as accepted.

 

References: Hyde et al. 2013 (morphology, taxonomy), Jayawardena et al. 2014, Fan et al. 2017 (morphology, phylogeny), Chung and Liao 2008, Surup et al. 2018 (Phytotoxin).

 

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

Species Isolate ITS LSU RPB2 TEF1-α
Elsinoe abutilonis CBS 510.50* KX887185 KX886949 KX887068 KX886831
E. ampelina CBS 208.25 KX887186 KX886950 KX887069 KX886832
E. anacardii CBS 470.62* KX887189 KX886953 KX887072 KX886835
E. annonae CBS 228.64 KX887190 KX886954 KX887073 KX886836
E. arachidis CBS 511.50* KX887191 KX886955 KX887074 KX886837
E. arrudai CBS 220.50* KX887194 KX886958 KX887077 KX886840
E. asclepiadea CPC 18544* = RWB1202 = CBS 141937 KX887195 KX886959 KX887078 KX886841
E. australis CBS 314.32* KX887198 KX886962 KX887081 KX886844
E. banksiicola CBS 113734* = CPC1508 = CPC 1510 KX887199 KX886963 KX887082 KX886845
E. barleriicola CBS 471.62* = ATCC 14658 KX887200 KX886964 KX887083 KX886846
E. bidentis CBS 512.50* KX887201 KX886965 KX887084 KX886847
E. brasiliensis CPC 18528 = RWB 1133 KX887204 N/A KX887087 KX886850
E. caleae CBS 221.50* KX887205 KX886968 KX887088 KX886851
E. centrolobii CBS 222.50* KX887206 KX886969 KX887089 KX886852
E. citricola CPC 18535* = RWB 1175 KX887207 KX886970 KX887090 KX886853
E. coryli CBS 275.76* KX887209 KX886972 KX887092 KX886855
E. diospyri CBS 223.50* KX887210 KX886973 KX887093 KX886856
E. embeliae CBS 472.62* KX887211 KX886974 N/A KX886857
E. erythrinae CPC 18542* = RWB 1196 KX887214 KX886977 KX887096 KX886860
E. eucalypticola CBS 124765* = CPC 13318 KX887215 KX886978 KX887097 KX886861
E. eucalyptorum CBS 120084* = CPC 13052 KX887216 KX886979 KX887098 KX886862
E. euphorbiae CBS 401.63* KX887217 KX886980 KX887099 KX886863
E. fagarae CBS 514.50* KX887218 KX886981 KX887100 KX886864
E. fawcettii CBS 139.25* KX887219 KX886982 KX887101 KX886865
E. fici CBS 515.50 KX887223 KX886986 KX887105 KX886869
E. fici-caricae CBS 473.62* = ATCC 14652 KX887224 KX886987 KX887106 KX886870
E. flacourtiae CBS 474.62* = ATCC 14654 KX887225 KX886988 KX887107 KX886871
E. freyliniae CBS 128204* = CPC 18335 KX887226 KX886989 KX887108 KX886872
E. genipae CBS 342.39* KX887227 KX886990 KX887109 KX886873
E. genipae-americanae CBS 516.50* KX887228 KX886991 KX887110 KX886874
E. glycines CBS 389.64* KX887229 KX886992 KX887111 KX886875
E. hederae CBS 517.50* KX887231 KX886994 KX887113 KX886877
E. ichnocarpi CBS 475.62* = ATCC 14655 KX887232 KX886995 KX887114 KX886878
E. jasminae CBS 224.50* KX887233 KX886996 KX887115 KX886879
E. jasminicola CBS 212.63* KX887234 KX886997 N/A KX886880
E. krugii CPC 18531* = RWB 1151 KX887235 KX886998 KX887116 KX886881
E. lagoa-santensis CBS 518.50* KX887239 KX887002 KX887120 KX886885
E. ledi CBS 167.33* KX887240 KX887003 KX887121 KX886886
E. lepagei CBS 225.50* KX887241 KX887004 KX887122 A
E. leucospermi CBS 111207* = CPC 1380 KX887242 KX887005 KX887123 KX886887
E. lippiae CBS 166.40* KX887248 KX887011 KX887129 KX886893
E. mangiferae CBS 226.50* KX887249 KX887012 KX887130 KX886894
E. mattiroloanum CBS 287.64 KX887250 KX887013 KX887131 KX886895
E. menthae CBS 322.37* KX887253 KX887016 KX887134 KX886898
E. mimosa CPC 19478* KX887255 KX887018 KX887136 KX886900
E. oleae CBS 227.59* KX887256 KX887019 KX887137 KX886901
E. othonnae CBS 139910* = CPC 24853 N/A N/A N/A N/A
E. perseae CBS 406.34* KX887258 KX887021 KX887139 KX886903
E. phaseoli CBS 165.31* KX887263 KX887026 KX887144 KX886908
E. piri CBS 163.29 KX887267 KX887030 KX887148 KX886912
E. pitangae CBS 227.50* KX887269 KX887032 KX887150 KX886914
E. poinsettiae CBS 109333 KX887270 KX887033 KX887151 KX886915
E. pongamiae CBS 402.63* KX887272 KX887035 KX887153 KX886917
E. populi CBS 289.64 KX887273 KX887036 KX887154 KX886918
E. proteae CPC 1349* N/A N/A N/A N/A
E. protearum CBS 113618* KX887275 KX887038 KX887156 KX886920
E. punicae CPC 19968 KX887276 KX887039 KX887157 KX886921
E. quercus-ilicis CBS 232.61* KX887277 KX887040 N/A KX886922
E. randii CBS 170.38* KX887278 KX887041 KX887158 KX886923
E. rhois CBS 519.50* KX887280 KX887043 KX887160 KX886925
E. ricini CBS 403.63 = ATCC 15030 KX887281 KX887044 KX887161 KX886926
E. rosarum CBS 212.33* KX887283 KX887046 KX887163 KX886928
E. salicina CPC 17824* KX887286 KX887049 KX887166 KX886931
E. semecarpi CBS 477.62* = ATCC 14657 KX887287 KX887050 KX887167 KX886932
E. sesseae CPC 18549 = RWB 1219 KX887288 KX887051 KX887168 KX886933
E. sicula CBS 398.59* KX887289 KX887052 KX887169 KX886934
E. solidaginis CBS 191.37* KX887290 KX887053 KX887170 KX886935
Elsinoë sp. CBS 128.14 KX887291 KX887054 KX887171 KX886936
E. tectificae CBS 124777* = CPC 14594 KX887292 KX887055 KX887172 KX886937
E. terminaliae CBS 343.39* KX887293 KX887056 KX887173 N/A
E. theae CBS 228.50* KX887295 KX887058 KX887175 KX886939
E. tiliae CBS 350.73 = ATCC 24510 KX887296 KX887059 KX887176 KX886940
E. veneta CBS 164.29* = ATCC 1833 KX887297 KX887060 KX887177 KX886941
E. verbenae CPC 18561* = RWB 1232 KX887298 KX887061 KX887178 KX886942
E. violae CBS 336.35* KX887302 KX887065 KX887182 KX886946
E. zizyphi CBS 378.62* = ATCC 14656 KX887303 KX887066 KX887183 KX886947
Myriangium hispanicum CBS 247.33 KX887304 KX887067 KX887184 KX886948

Phylogenetic tree generated by maximum Parsimony analysis of combined ITS, LSU, RPB2 and TEF1-α sequence data of Elsinoe species. Related sequences were obtained from GenBank. Seventy five strains are included in the analyses, which comprise 2479 characters including gaps. Single gene analyses were carried out (not shown) and the phylogeny generated were the same as combined analyses. Tree was rooted with Myriangium hispanicum (CBS 247.33). The maximum parsimonious dataset consisted of 1623 constant, 653 parsimony-informative and 203 parsimony-uninformative characters. The parsimony analysis of the data matrix resulted in the maximum of ten equally most parsimonious trees with a length of 4748 steps (CI = 0.298, RI 0.699, RC = 0.208, HI = 0.702) in the first tree. Bayesian posterior probabilities and MP bootstrap values ≥ 50 % are shown respectively near the nodes. The scale bar indicates 0.2 changes. The ex-type strains are in bold.

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