Interspecific and intraspecific diversity in oak powdery mildews in Europe: coevolution history and adaptation to their hosts

Quercus has been reported as the genus with the largest number of attacking powdery mildews. In Europe, oak powdery mildew was rarely reported before 1907, when severe outbreaks were observed. These epidemics were attributed to the newly described species Erysiphe alphitoides, presumed to be of exotic origin. After the burst of interest following the emergence of the disease, research on this topic remained very limited. Interest in research was recently reactivated in response to the availability of molecular tools. This review summarizes current knowledge on the diversity of oak powdery mildews in Europe and their possible evolutionary relationships with European oaks. The most striking results are the evidence of cryptic diversity (detection in France of a lineage closely related to Erysiphe quercicola, previously thought to only have an Asian distribution), large host range (similarity of E. alphitoides and E. quercicola with powdery mildews of tropical plants) but also local adaptation to Quercus robur. These recent findings highlight the complexity of the history of oak powdery mildew in Europe and point to the question of host specialization and host jumps in the evolution of powdery mildew fungi.     

Powdery mildews (Ascomycota,Erysiphales) on Fontanesia phillyreoides and Jasminum fruticans in Turkey

Asexual and sexual morphs of powdery mildews on Fontanesia phillyreoides and Jasminum fruticans, two hitherto unknown host species, have recently been collected in Turkey. Analyses of morphological traits and molecular sequence data led to identifications of the causal agents of the powdery mildew diseases involved. Fontanesia phillyreoides was infected by Phyllactinia fraxini, and the powdery mildew on Jasminum fruticans can be classified as Erysiphe cf. aquilegiae. The latter host showed traces of a co-infection with a second powdery mildew (only asexual morph) belonging to the genus Phyllactinia (= Ovulariopsis) and morphologically well agreeing with P. fraxini.     

Sawadaea nankinensis comb. nov.: a powdery mildew fungus of Acer buergerianum

The anamorphic state of a powdery mildew on trident maple (Acer buergerianum, Aceraceae), belonging to Sawadaea, has been observed since 1980 in Tokyo and other areas of Japan. Since the autumn of 2003, this fungus has begun to produce chasmothecia in various areas of Japan, which were consistent with Erysiphe nankinensis (= Uncinula nankinensis), but apparently contradictory to the characteristics of the anamorph. Based on a molecular phylogenetic analysis using DNA separately extracted from the anamorph and teleomorph of the fungus on A. buergerianum, it could be demonstrated that sequences of this fungus are sister to Sawadaea. As the anamorph belongs to Oidium subgen. Octagoidium and because of the phylogenetic position within the Sawadaea clade, the new combination Sawadaea nankinensis is proposed for this species. The genus Sawadaea is emended to comprise species with consistently unbranched appendages.     

Molecular phylogenetic analyses reveal a close relationship between powdery mildew fungi on some tropical trees and Erysiphe alphitoides, an oak powdery mildew

To investigate the phylogenetic relationships among the powdery mildew fungi of some economically important tropical trees belonging to Oidium subgenus Pseudoidium, we conducted molecular phylogenetic analyses using 30 DNA sequences of the rDNA internal transcribed spacer (ITS) regions and 26 sequences of the domains D1 and D2 of the 28S rDNA obtained from the powdery mildews on Hevea brasiliensis (para rubber tree), Anacardium occidentale (cashew), Bixa orellana, Citrus spp., Mangifera indica (mango), and Acacia spp. The results indicate that the powdery mildew fungi isolated from these tropical trees are closely related to one another. These powdery mildews are also closely related to E. alphitoides (including Erysiphe sp. on Quercus phillyraeoides). Because of the obligate biotrophic nature of the powdery mildew fungi, the relationship between powdery mildews and their host plants is conservative. However, the present study suggests that a particular powdery mildew species has expanded its host ranges on a wide range of the tropical trees. This article also suggests that a powdery mildew fungus distributed in temperate regions of the Northern Hemisphere expanded its host ranges onto tropical plants and may be a good example of how geographical and host range expansion has occurred in the Erysiphales.     

The First Record and Characterization of Powdery Mildew (Erysiphe pachypodiae sp. nov.) on Pachypodium lamerei (Apocynaceae)

During the summer and autumn of 1999, symptoms of powdery mildew disease were first observed on Pachypodium lamerei in the Czech Republic. White lesions of irregular shape appeared on leaf margins and spread towards the central vein of the leaf, often followed by necrosis of leaf tissue. In the spring of 2000, the sexual stage (cleistothecia) also appeared on infected leaves. Based on the observations of the morphology of its anamorph and teleomorph stage as well as on results from inoculation experiments, the identity and origin of this powdery mildew species are discussed. Based on the pseudoidium anamorph, this fungus may be clearly assigned to Erysiphe emendation, probably to section Uncinula, since the cleistothecial appendages are non‐mycelioid and occassionally circinate at the apex. The fungus is described as a new species Erysiphe pachypodiae sp. nov.     

First record of <Emphasis Type="Italic">Erysiphe magnifica</Emphasis> on lotus,a host outside the Magnoliales

The powdery mildew Erysiphe magnifica (Erysiphales, Ascomycota) has been recorded for the first time on lotus (Nelumbo nucifera) based on a collection from the Botanical Garden in Frankfurt am Main, Germany. This powdery mildew previously known only from Magnolia species was identified by a combination of light and scanning electron microscopic investigation of ascomata and the Oidium stage, and comparison of ITS DNA sequences. This finding is discussed with respect to the narrow host specificity concept used in Erysiphales taxonomy, the effect of lotus leaf surface on fungal infection, and the extending geographical distribution of powdery mildews.     

Niche partitioning of the genetic lineages of the oak powdery mildew complex

Recent molecular studies have shown that four genetic lineages, probably cryptic species, cause oak powdery mildew in Europe. We tested the hypothesis of niche differentiation between the two most frequent species (Erysiphe alphitoides and Erysiphe quercicola), by determining their relative prevalences at various times during the growing season. E. quercicola was strictly associated with the flag-shoot symptom in a 2-yr sampling campaign of 35 natural oak seedling populations. Additional sampling during Aug.–Sep. in the same stands showed that E. alphitoides predominated in most (70 %) cases. Time-course monitoring of powdery mildew in two natural regenerating oak populations confirmed the inverse patterns of relative abundance for these two species in early and late season. The coexistence of these two closely related species may be due to the use of different strategies, resulting from a trade-off between overwintering (flag-shoots vs. chasmothecia) and late-season performance.     

Molecular phylogenetic and morphological analyses of Oidium heveae, a powdery mildew of rubber tree

Powdery mildew of rubber tree caused by Oidium heveae is an important disease of rubber plantations worldwide. Identification and classification of this fungus is still uncertain because there is no authoritative report of its morphology and no record of its teleomorphic stage. In this study, we compared five specimens of the rubber powdery mildew fungus collected in Malaysia, Thailand, and Brazil based on morphological and molecular characteristics. Morphological results showed that the fungus on rubber tree belongs to Oidium subgen. Pseudoidium. Nucleotide sequence analysis of the ribosomal DNA internal transcribed spacer (ITS) region and the large subunit rRNA gene (28S rDNA) were conducted to determine the relationships of the rubber powdery mildew fungus and to link this anamorphic fungus with its allied teleomorph. The results showed that the rDNA sequences of the two specimens from Malaysia were identical to a specimen from Thailand, whereas they differed by three bases from the two Brazilian isolates: one nucleotide position in the ITS2 and two positions in the 28S sequences. The ITS sequences of the two Brazilian isolates were identical to sequences of Erysiphe sp. on Quercus phillyraeoides collected in Japan, although the 28S sequences differed at one base from sequences of this fungus. Phylogenetic trees of both rDNA regions constructed by the distance and parsimony methods showed that the rubber powdery mildew fungus grouped with Erysiphe sp. on Q. phillyraeoides with 100% bootstrap support. Comparisons of the anamorph of two isolates of Erysiphe sp. from Q. phillyraeoides with the rubber mildew did not reveal any obvious differences between the two powdery mildew taxa, which suggests that O. heveae may be an anamorph of Erysiphe sp. on Q. phillyraeoides. Cross-inoculation tests are required to substantiate this conclusion.     

Mapping resistance to powdery mildew in barley reveals a large-effect nonhost resistance QTL

Key message

Resistance factors against non-adapted powdery mildews were mapped in barley. Some QTLs seem effective only to non-adapted mildews, while others also play a role in defense against the adapted form.The durability and effectiveness of nonhost resistance suggests promising practical applications for crop breeding, relying upon elucidation of key aspects of this type of resistance. We investigated which genetic factors determine the nonhost status of barley (Hordeum vulgare L.) to powdery mildews (Blumeria graminis). We set out to verify whether genes involved in nonhost resistance have a wide effectiveness spectrum, and whether nonhost resistance genes confer resistance to the barley adapted powdery mildew. Two barley lines, SusBgt_SC and SusBgt_DC, with some susceptibility to the wheat powdery mildew B. graminis f.sp. tritici (Bgt) were crossed with cv Vada to generate two mapping populations. Each population was assessed for level of infection against four B. graminis ff.spp, and QTL mapping analyses were performed. Our results demonstrate polygenic inheritance for nonhost resistance, with some QTLs effective only to non-adapted mildews, while others play a role against adapted and non-adapted forms. Histology analyses of nonhost interaction show that most penetration attempts are stopped in association with papillae, and also suggest independent layers of defence at haustorium establishment and conidiophore formation. Nonhost resistance of barley to powdery mildew relies mostly on non-hypersensitive mechanisms. A large-effect nonhost resistance QTL mapped to a 1.4 cM interval is suitable for map-based cloning.

     

Powdery Mildew Caused by an Erysiphe sp. on Korean Ginseng

In August and September 2014, Korean ginseng (Panax ginseng) plants showing symptoms of powdery mildew infection were found in a polyethylene film‐covered greenhouse in Suwon, Korea. The mildew was initially observed to occur in circular to irregular white colonies, which subsequently developed into abundant mycelial growths on both leaf surfaces. No chasmothecia were observed. Based on its morphological characteristics, the fungus was determined to be a species of Erysiphe. Phylogenetic analysis of the sequence of the internal transcribed spacer region of the ribosomal DNA obtained from the isolate placed the powdery mildew fungus in the genus Erysiphe. Here, we describe this Erysiphe sp. found growing on Korean ginseng using both illustrations and molecular data. A comparison of the Korean isolate and three previous records of powdery mildews known to grow on Panax plants is also provided. This is the first report of powdery mildew on Korean ginseng in Korea.     

Characterization of six polymorphic microsatellite loci from Ampelomyces quisqualis,intracellular mycoparasite and biocontrol agent of powdery mildew

Ampelomyces spp. are common intracellular mycoparasites of powdery mildews worldwide and a strain has been commercialized as a biocontrol agent against these plant pathogens. In light of recent genetic analyses revealing high internal transcribed spacer sequence variability among Ampelomyces strains on different host plant mildews, yet no sequence variability within the Malus strain, polymorphic microsatellites were required to permit biocontrol and ecological studies of the complex apple/apple mildew/Ampellomyces tritrophic interaction. For this purpose, described here are the primers to amplify six polymorphic microsatellite loci from Ampelomyces quisqualis isolated from mycelia of the apple powdery mildew fungus, Podosphaera leucotricha.     

Four powdery mildew species with catenate conidia infect Galium: molecular and morphological evidence

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.     

Natural genetic differentiation and human-mediated gene flow: the spatiotemporal tendency observed in a long-lived <Emphasis Type="Italic">Cinnamomum camphora</Emphasis> (Lauraceae) tree

The camphor tree (Cinnamomum camphora) is an important natural resource in East Asia. From the early eighteenth to mid-twentieth century, C. camphora was widely cultivated to obtain camphor, a white crystalline substance used as a repellent, a component of medicine, and an ingredient in the production of smokeless gunpowder and celluloid. The vast utilization and cultivation of C. camphora have obscured its natural distribution, and the genetic structure of this species was likely affected by both natural factors and human activities in different areas and at different times. To estimate this process, we collected 817 samples from Japan, China, and Taiwan, including samples from trees estimated to be hundreds to thousands of years old. Population genetic analyses using 11 microsatellite markers detected the footprints of ancient genetic differentiation and recent human-mediated gene flow. The strong genetic differentiation between areas (Japan vs. China and Taiwan) and the decreased genetic diversity in Japan can be ascribed to the long-term geographical isolation during and after the glacial period. Within each area, the genetic composition of the cultivated or planted populations was often inconsistent with the surrounding natural and/or older specimens. This finding may be due to the regional transfer of plant materials with no regard to their genetic origin. We also detected rare but evident immigration from different areas; furthermore, these non-native genets seemed to locally hybridize with the native genets. We suggest that the intentional transfer and/or artificial hybridization between areas should be prohibited in order to preserve the genetic composition of C. camphora.     

伞房决明白粉病的初次报道(英文)

伞房决明是长江三角洲地区的园林绿化木本植物,在每年8月下旬至11月中旬会发生严重的白粉病,造成提前落叶,导致次年部分植株死亡。该病由Oidium cassiae-siameae引起。经过3年多的野外观察,未发现有性世代。初次报道伞房决明为Oidium cassiae-siameae白粉菌的新寄主。此真菌为中国大陆的初次记载。     

Molecular data do not support a southern hemisphere base of Nothofagus powdery mildews

Three powdery mildew species present on Nothofagus (viz. Erysiphe magellanica, E. nothofagi and E. patagoniaca) are endemic to South America and have unique ascomatal appendages that are not found in powdery mildews of the northern hemisphere. We determined the nucleotide sequences of the rDNA internal transcribed spacer regions and D1/D2 domains of the 28S rDNA of these three powdery mildew species to reveal their phylogenetic relationships with powdery mildews of the northern hemisphere. Although the molecular phylogenetic analyses indicated that the three Nothofagus powdery mildews are closely related to each other they did not group into one clade in either the ITS or 28S trees. Kishino-Hasegawa, Shimodaira-Hasegawa and Templeton tests could not significantly reject the constrained trees that were constructed based on the assumption that the Nothofagus powdery mildews would form a single clade. Based on this result and the evidence that all Nothofagus powdery mildews are endemic to South America and have similar morphological characteristics, it is likely that these three species diverged from a single ancestor present on Nothofagus. Calibration of evolutionary events with molecular clocks suggested that the Nothofagus powdery mildews split from the northern hemisphere relatives 22-16 million y ago (Ma) in the middle Miocene, and divergence among the Nothofagus powdery mildews occurred 17-13 Ma. These results do not support a southern hemisphere base of the Nothofagus powdery mildews.     

<Emphasis Type="Italic">Erysiphe catalpae</Emphasis> and <Emphasis Type="Italic">Erysiphe elevata</Emphasis> in Europe

The recent epidemic spread of the North American powdery mildew Erysiphe elevata in Europe is described and discussed. Since 2002, this plant pathogenic fungus has been collected on Catalpa bignonioides, C. erubescens and C. speciosa in the Czech Republic, Germany, Hungary, Slovakia and Switzerland. The diagnostically important anamorph of E. elevata, so far unknown, is described and illustrated in detail. Type material of Erysiphe catalpae and two specimens of E. catalpae recently collected in Poland have been examined and compared with E. elevata. The anamorph as well as the teleomorph of E. catalpae proved to be easily distinguishable from E. elevata. The supposition that E. catalpae, introduced in Armenia, was based on immature ascomata of E. elevata proved to be wrong. The origin and distribution of E. catalpae are discussed, and a key to powdery mildew fungi on Catalpa spp. in Europe is provided.     

Use of holomorph characters to delimit Microascus nidicola and M. soppii sp. nov., with notes on the genus Pithoascus

Several isolates of a perithecial microascaceous ascomycete having falcate ascospores and a Scopulariopsis anamorph were obtained from rotting wood in the boreal forest of Alberta, Canada. Additional isolates appeared conspecific based on anamorphic characters, but failed to produce a teleomorph. These isolates showed similarities to Microascus nidicola (type species of the genus Pithoascus) and Scopulariopsis flava. Sexual compatibility systems were investigated to establish holomorph concepts for these taxa. The teleomorph obtained in mating trials among anamorphic isolates was identical to that of self-fertile isolates. The new heterothallic species M. soppii is described. The anamorph is S. soppii. Single ascospore isolates derived from M. nidicola demonstrated homothallism and lacked an anamorph. Scopulariopsis flava (basionym Acaulium flavum) is considered a nomen dubium. Generic concepts of Pithoascus are evaluated and the genus is treated as a synonym of Microascus. Pithoascus stoveri is transferred as M. stoveri comb. nov.     

Constraints to the development of biofungicides: The example of “AQ10”, a new product for controlling powdery mildews

Over recent years, the company ECOGEN Inc. has been successfully developing a biofungicide known under the trade name ‘AQ10’ in the USA where it has been authorized in 1994 for controlling powdery mildews on various host plants. This new product is based on the use ofAmpelomyces quisqualis, an hyperparasitic fungal species infesting representatives ofErysiphaceae (powdery mildews) only. The production process now allows for the hyperparasite to be mass-cultured and formulated into an easily water-dispersed, dry powder which preserves spore viability at room temperature for a period in excess of 12 months. Upon spraying, the conidia germinate rapidly to effectively attack any developing powdery mildew colonies. Efforts are now concentrating on experimental application schedules in vineyards aimed at defining an optimal positioning of the biofungicide within existing disease control programmes. The pilot trials are being conducted over a large number of wine-producing areas under a Mediterranean climate around the world where powdery mildew represents the major pest problem. Results obtained so far show that in order to achieve an optimal, cost-effective, consistent disease control, the biofungicide has to be applied before the incidence of powdery mildew has reached high levels, and at any of the three most susceptible growth stages of grapevine,i.e. bud break, between flowering and bunch closure, and just before veraison. The biofungicide may therefore be used as a curative to slightly preventative control agent likely to fit into any IPM strategies. The various technical problems associated with the development and industrial production of this new biofungicide are largely solved. Constraints relating to designing comprehensive, user-friendly IPM programmes which include ‘AQ10’ still require adjustments in terms of defining spraying dates and intervals according to a range of agricultural practices, climatic changes likely to occur during the season, and compatibility for tank-mixing with other pesticides. A number of additional constraints relate to official registration in various countries, distributors’ and farmers’ acceptance of a new, ‘living’ product: these are still more difficult to address because they claim for a profound change in the users’ general attitude towards controlling diseases of cultivated plants.