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Phylogenetic connections among genera of powdery mildew fungi and some questions of systematics of Erysiphales

Authors:
  • M.G.Kholodny Institute of Botany, National Academy of Sciences of Ukraine

Abstract

Phylogenetic connections among 20 teleomorphic genera of powdery mildew fungi are discussed. A new system of the order Erysiphales is proposed. The order is divided into three families (Blumeriaceae, Erysiphaceae and Leveillulaceae), four families (Erysiphoideae, Golovinomycetoideae, Leveilluloideae, and Phyllactinioideae) and several tribes. Section Golovinomyces U. Braun is raised to the rank of the genus.
... Later, the genus Erysiphe was divided into three genera, viz. Erysiphe s. str., Golovinomyces and Neoerysiphe, based on characteristics of the anamorph, as well as on molecular phylogenetic analyses (Heluta 1988;Braun 1999). Erysiphe galii var. ...
... galii was reassessed as N. galii (Braun 1999) and E. galii var. riedliana was reapproved as G. riedlianus (Heluta 1988). However, the validity of this taxonomic treatment has not yet been proven using DNA sequence analyses. ...
... The other three groups belong to the genus Golovinomyces. Therefore, this study supports the taxonomic revision of Heluta (1988Heluta ( , 1989 and Braun (1999) in which the powdery mildews of Galium include both Golovinomyces and Neoerysiphe species. Moreover, the present study indicates that the fungi belonging to Golovinomyces can be divided into three groups. ...
Article
The Erysiphaceae are a group of obligately biotrophic fungi that cause powdery mildew disease of angiosperms. Due to their inability to be cultured on artificial media, the taxonomy of the Erysiphaceae has generally been based on the morphological characteristics of fresh and herbarium specimens. Thus, several morphological species with wide host ranges have long been maintained in this family, even though they clearly consist of several biological species. Erysiphe galii has been known as a powdery mildew of Galium spp. Recently, the former E. galii var. galii has been reassessed as Neoerysiphe galii and E. galii var. riedliana as Golovinomyces riedlianus, along with a taxonomic revision of the generic concept of the Erysiphaceae. The present study was conducted to evaluate the validity of the taxonomic revision of the two varieties of E. galii. During the course of this study, we found that the Galium powdery mildews consist of at least four different species, viz. Neoerysiphe galii, Golovinomyces orontii, G. riedlianus, and an unknown species collected in Argentina. The latter species is described as a new species, Golovinomyces calceolariae. The three species belonging to Golovinomyces are morphologically very similar to each other, i.e. the discrimination between them is rather difficult. The morphological differences of the three Golovinomyces species of Galium are discussed.
... Previously, the genus Neoerysiphe was classified as section Galeopsidis within the genus Erysiphe s. lat. Because molecular phylogenetic analyses revealed that Erysiphe s. lat. is polyphyletic (Takamatsu et al. 1998;Saenz & Taylor 1999), the sections Galeopsidis, Erysiphe, and Golovinomyces have been raised up to generic rank (Heluta 1988;Braun 1999). The genus Neoerysiphe belongs to the tribe Golovinomyceteae together with the genera Arthrocladiella and Golovinomyces. ...
... riedliana) of E. galii (Braun 1987(Braun , 1995. The two varieties were considered as two different species, Golovinomyces galii and G. riedlianus, by Heluta (1988Heluta ( , 1989. G. galii was later revised as N. galii in the taxonomic revision conducted by Braun (1999). ...
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The genus Neoerysiphe belongs to the tribe Golovinomyceteae of the Erysiphaceae together with the genera Arthrocladiella and Golovinomyces. This is a relatively small genus, comprising only six species, and having ca 300 species from six plant families as hosts. To investigate the molecular phylogeny and evolution of the genus, we determined the nucleotide sequences of the rDNA ITS regions and the divergent domains D1 and D2 of the 28S rDNA. The 30 ITS sequences from Neoerysiphe are divided into three monophyletic groups that are represented by their host families. Groups 1 and 3 consist of N. galeopsidis from Lamiaceae and N. galii from Rubiaceae, respectively, and the genetic diversity within each group is extremely low. Group 2 is represented by N. cumminsiana from Asteraceae. This group also includes Oidium baccharidis, O. maquii, and Oidium spp. from Galinsoga (Asteraceae) and Aloysia (Verbenaceae), and is further divided into four subgroups. N. galeopsidis is distributed worldwide, but is especially common in western Eurasia from Central Asia to Europe. N. galii is also common in western Eurasia. In contrast, the specimens of group 2 were all collected in the New World, except for one specimen that was collected in Japan; this may indicate a close relationship of group 2 with the New World. Molecular clock calibration demonstrated that Neoerysiphe split from other genera of the Erysiphaceae ca 35-45M years ago (Mya), and that the three groups of Neoerysiphe diverged between 10 and 15Mya, in the Miocene. Aloysia citriodora is a new host for the Erysiphaceae and the fungus on this plant is described as O. aloysiae sp. nov.
... Powdery mildew (PM) is probably the most destructive disease affecting cucurbitaceous plants worldwide. It is caused by Podosphaera xanthii (Castagne) U. Braun and N. Shishkoff (Sphaerotheca fuliginea Schlech previously ex Fr.Poll.) and Golovinomyces orontii (Castagne) (Golovinomyces cichoracearum or Erysiphe cichoracearum DC ex Merate) (Heluta, 1988;Bardin et al., 1999;Braun and Takamutsu, 2000;Lebeda and Sedláková, 2010;Pirondi et al., 2015). Podosphaera xanthii is a major problem in many countries of the world among the diseases affecting melon crops (Robinson and Decker-Walters, 1997;Kuzuya et al., 2006;Wang et al., 2011). ...
... Cucurbit powdery mildew is one of the most common, devasting, conspicuous, and widespread diseases of cucurbit crops. Powdery mildew dis-eases on cucurbits are caused by two obligate biotrophic pathogens Golovinomyces orontii (Castagne) Heluta (1988) and Podosphaera xanthii (Castagne) U. Braun and N. Shishkoff (Braun and Takamatsu 2000). Like other powdery mildew species, G. orontii produces signals on plant surfaces characterized by abundant whitish, talcum-like fungal spores on both sides of the leaves as well as on stems and petioles (Qui et al. 2018). ...
Article
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This study presents the development of species-specific PCR primers for detection of Golovinomyces orontii, the causal agent of powdery mildew disease on different cucurbit hosts. The species-specific primers CgF2 and CgR2 were designed based on partial ITS and 5.8S rDNA sequences using an isolates collection of powdery mildew and downy mildew pathogens from different sources. After optimization of the PCR conditions, a 233 bp fragment was amplified only from DNA of G. orontii. Limit of detection was determined to be 0.01 ng of pure conidial genomic DNA. Further association of PCR and high-resolution melting (HRM) analysis showed that the designed primer set can be used for differentiation of G. orontii from different powdery mildew fungi in infected cucurbits tissue collected in the field.
... After the section Golovinomyces U. Braun (genus Erysiphe R. Hedw. ex DC.) was raised to the genus level (Heluta 1988a), the species was transferred to this genus and named G. cumminsianus (U. ...
Article
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Information is provided about the distribution of a powdery mildew fungus species new for Israel, Neoerysiphe cumminsiana (U. Braun) U. Braun (Erysiphales), recorded on Crepis spp. and Phagnalon rupestre (L.) DC. A conclusion is reached about the possibility of discovering this fungus in some countries of southern Europe and in northern and southern Africa. The need is noted for the revision of powdery mildew specimens identified as Erysiphe cichoracearum DC. and collected in these regions on host plants belonging to Asteraceae.
... Among the over 200 diseases affecting cucurbits (Zitter et al. 1996), powdery mildew is considered the most important widespread disease limiting cucurbit production. Although there are some indications of records of Leveillula taurica as a causal species of cucurbit powdery mildew (El Ammari & Wajid Khan 1983;Branzanti & Brunelli 1992;Vakalounakis et al. 1994), the most common pathogens causing the disease are two obligate biotrophic ascomycetes fungi: Podosphaera xanthii (Castagne) U. Braun and N. Shishkoff (Braun & Takamatsu 2000) and Golovinomyces orontii (Castagne) Heluta (1988). In the North of Italy, as in many areas of the world, P. xanthii is the predominant species causing cucurbit powdery mildew (Branzanti & Brunelli 1992;Pirondi et al. 2015a). ...
Article
The sexual stage of Podosphaera xanthii is rarely found worldwide. However, chasmothecia are frequently recorded in northern Italy, suggesting the presence of an actively mating population. With the aim of investigating the genetic structure of the Italian population with respect to populations from other countries, genetic diversity analysis was performed both on 92 isolates from European and American countries by multilocus sequence typing (MLST) and on 59 isolates by amplified fragment length polymorphism (AFLP) methods. Mating type frequencies were tested for random mating and two-locus linkage disequilibrium (LD) analysis was performed. Results showed very low levels of genetic diversity: MLST showed no variations in eight housekeeping gene fragments and, accordingly, UPGMA dendrogram from AFLP data showed a high similarity (0.91-1.00 simple matching similarity coefficient) between isolates. Moreover, the random mating test showed no deviations from mating-type 1:1 ratio in the Italian population but deviations were observed in populations from Europe and American countries while two-locus LD analysis showed the presence of significant LD. The results suggest that the populations of P. xanthii are likely to be predominantly clonal, and asexual reproduction, producing a huge amount of conidia, appears to be the predominant type of reproduction of the species. Copyright © 2015 The British Mycological Society. Published by Elsevier Ltd. All rights reserved.
... Cucurbit powdery mildew is probably the most important disease affecting cucurbitaceous plants worldwide. The disease is caused by two obligate biotrophic pathogens: Podosphaera xanthii (Castagne) U. Braun and N. Shishkoff (Braun & Takamatsu, 2000) and Golovinomyces orontii (Castagne) V.P. Heluta (1988). Both powdery mildews belong to Phylum Ascomycota, Subdivision Pezizomycotina, Class Leotiomycetes, Order Erysiphales and Family Erysiphaceae (Wang et al., 2006;Braun & Cook, 2012). ...
Article
Powdery mildew, caused by Golovinomyces orontii and Podosphaera xanthii, is a widespread disease that causes important losses in cucurbit production. To determine the aetiology and the epidemiology of cucurbit powdery mildew disease in the North of Italy, observations on the occurrence of the main disease-causing fungal species were conducted during the 2010, 2011 and 2012 growing seasons. Samples of infected leaves of zucchini, melon and pumpkin plants, either from field or greenhouse crops, were collected every 15–18 days from May to September/October. To identify the fungal species, both morphological observations based on the asexual stage and molecular identifications by a Multiplex-PCR reaction with species-specific primers were performed. Climatic parameters of temperature and relative humidity were also monitored. Pearson's correlation coefficient and Principal Component Analysis showed a negative significant correlation between the two species, and a peculiar epidemiological behaviour was also observed: the earlier infections were caused by G. orontii, which was the predominant species till the end of June–middle of July. At this time, this species progressively decreased in frequency and was replaced by P. xanthii that became the main species infecting cucurbits till the end of the growing season. As the two species have different ecological requirements, these seasonal variations in the cucurbit powdery mildew species composition could possibly be explained by the influence of temperature and relative humidity on the pathogen epidemiology during the growing season but also by the different overwintering strategies adopted by the two species.
... The disease can be caused by the ascomycetes fungi Podosphaera xanthii (Castagne) U. Braun et N. Shishkoff (Braun and Takamatsu, 2000) and Golovinomyces orontii (Castagne) V.P. Heluta (1988). Like many powdery mildews, both species are heterothallic and sexual development is controlled by a mating type (MAT) locus that occurs in two opposite forms, named idiomorphs: MAT 1-1-1 and MAT 1-2-1 (Brewer et al., 2011). ...
Article
Full-text available
Powdery mildew is a widespread disease that causes important losses to cucurbit production. The main agents of the disease are Podosphaera xanthii and Golovinomyces orontii. To determine the occurrence of chasmothecia as overwintering forms of both fungal species in northern Italy, powdery mildew-infected samples from cultivated cucurbits were collected in different locations of the provinces of Bologna and Mantova during 2010, 2011 and 2012. Only the sexual stage of P. xanthii was found, indicating that in northern Italy, contrary to what reported from other areas of the Mediterranean basin, the pathogen overwinters as chasmothecia. In parallel, to determine the frequency and distribution of both MAT 1-1-1 and MAT 1-2-1 P. xanthii idiomorphs, a multiplex- PCR with MAT idiomorph-specific primers was carried out on 147 monoconidial isolates obtained from infected leaf samples. The obtained frequencies were tested for random mating. Results showed a MAT ratio that tended to 1:1, supporting the finding of the sexual stage thus suggesting the occurrence of actively mating populations and that sexual reproduction plays a significant role in the life cycle of P. xanthii in this area. The lack of G. orontii chasmothecia suggests that this species might have alternative overwintering strategies.
... It was acknowledged that genera with a pseudoidium type of conidial formation (conidia mature one at a time) are obviously different from genera with a euoidium type of conidial formation (conidia mature gradually in a chain). Blumer (1933) and Gelyuta (1988) treated the euoidium type as primitive and the pseudoidium type as derived. In contrast, Braun (1987) regarded the pseudoidium type as primitive and the euoidium type as derived. ...
Article
This paper reviews the taxonomy, biology, importance, host–pathogen interactions and control of lettuce powdery mildew. The main causal agent of this disease, Golovinomyces cichoracearum s.s., is an important powdery mildew pathogen of many members of the family Asteraceae. The pathogen is distributed worldwide and occurs on Lactuca sativa as well as wild Lactuca spp. and related taxa (e.g. Cichorium spp.). Powdery mildew of lettuce can be a major problem in production areas with favourable environmental conditions for disease development (dry, hot weather). The fungus grows ectophytically and appears as white, powdery growth on both the upper and lower sides of leaves. There is rather limited information on the geographic distribution of powdery mildew on wild Lactuca spp. Most L. sativa cultivars have been found to be susceptible. Large variability in virulence was confirmed and existence of different races is supposed. Resistance in L. sativa and some related wild Lactuca spp. is characterized by race-specificity, but the genetic background of resistance is poorly understood. Sources of resistance are known in L. saligna and L. virosa. Lettuce powdery mildew can be effectively controlled by common fungicides (e.g. sulphur, myclobutanil, quinoline, strobilurins, etc.) and protective compounds (e.g. extract of neem oil, Reynoutria sachaliensis extracts). However, fungicide resistance may arise. Non-fungicidal activators of plant systemic acquired resistance (SAR) had no direct effect on the causal agent. Future issues regarding lettuce powdery mildew research are summarized.
... He confined the name 'E. cichoracearum' to fungi on Asteraceae. The genus Erysiphe was then split into three genera based on the morphology of the anamorph and on molecular analyses, and E. orontii was revised as G. orontii (Braun 1999;Heluta 1988). ...
Article
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In 2002, a powdery mildew with catenate conidia lacking fibrosin bodies was found on cucumber in a greenhouse in Kanagawa Prefecture, Japan. Morphological observation revealed that the fungus belongs to Oidium subgenus Reticuloidium, anamorph of the genus Golovinomyces. Molecular phylogenetic analyses of the nucleotide sequences of the rDNA ITS regions and D1/D2 domains of the 28S rDNA indicated that the fungus belongs to the clade of G. orontii with other Golovinomyces fungi from a wide range of host plants, suggesting that the fungus was newly transported from abroad. Because there has been no prior report of cucumber powdery mildew caused by Reticuloidium, further research on the physiology, epidemiology, control and resistant cucumber varieties is required.
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