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.     

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.     

Estimation of molecular clocks for ITS and 28S rDNA in Erysiphales

Based on a comparative phylogenetic analysis of Goloviomyces and their host tribes of the Asteraceae, we speculate that Golovinomyces first acquired parasitism to the Asteraceae after migration of the family into the Northern Hemisphere and before the divergence of the tribe Carduaeae. The divergence time of the Carduaeae is estimated to be 25.2Myr ago based on the molecular clock of rbcL sequences of the Asteraceae. When 25.2Myr is given at the node of the first split of the phylogenetic tree of Golovinomyces, nucleotide substitution rates of the Erysiphales are calculated to be 2.52 × 10^–9 per site per year (0.01D = 3.97Myr) in the ITS region and 6.5 × 10^–10 per site per year (0.01D = 15.4Myr) in the D1 and D2 regions of the 28S rDNA.     

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.     

Two new hosts of anamorphic Erysiphe quercicola: Cinnamomum camphora and Murraya paniculata

Based on collections of powdery mildews (Erysiphales) in Taiwan and combined molecular and morphological analyses, camphor tree (Cinnamomum camphora) and orange jasmine (Murraya paniculata) are recognized as new hosts of the anamorph of the powdery mildew Erysiphe quercicola. The anamorphic powdery mildew on C. camphora has been known as Pseudoidium cinnamomi, but its relationship to a teleomorph was unknown. For M. paniculata as substrate of powdery mildew, only an anamorphic Cystotheca species has been named. Morphological investigation of the fungus on this host shows that the specimens from Taiwan belong to another genus because of the lack of fibrosin bodies. Analysis of internal transcribed spacer sequences indicates that the anamorphic powdery mildews on camphor and orange jasmine belong to a clade representing E. quercicola, with the teleomorph found only on oak species (Quercus, Fagaceae), but with its anamorph reported from a broad host range, particularly in the tropics.     

Conidial germination patterns in powdery mildews

Four conidial germination types namely, polygoni (syn. Pseudoidium), cichoracearum (syn. Reticuloidium), pannosa (syn. Fibroidium) and fuliginea (syn. Magnicellulatae) are commonly used as an aid in the identification of the Oidium anamorphs of powdery mildews. However, results of germination tests and a survey of the literature showed that these types did not adequately distinguish all taxa and did not reflect the range of species covered. Hence two new main types, Striatoidium and Blumeria, are proposed for the newly created genus Neoerysiphe and for the unique pattern of B. graminis. Two new names, orthotubus and brevitubus subtypes of Fibroidium, are proposed for the pannosa and fuliginea types respectively. Also proposed is a special longitubus pattern for the long, undifferentiated, negatively hydrotropic germ tubes prevalent in Erysiphe trifolii and species in Golovinomyces sect. Depressi. The recognition of the Striatoidium type of N. galeopsidis as distinct from the Pseudoidium type of E. elevata facilitated the detection of a simultaneous infection of Catalpa by these two powdery mildews. A key is provided for the identification of Oidium genera based on germination types. A review of germination patterns in the tribe Phyllactinieae found no consistent differences amongst the genera. Golovinomyces sect. Depressi is re-described to accommodate Golovinomyces spp. often having a longitubus pattern of germination. It includes G. cichoracearum var. latisporus, now considered a separate species based on its germination type, other anamorphic morphology and previous molecular sequence analyses. A new combination, Golovinomyces ambrosiae, is proposed for this species. Other anomalies within G. cichoracearum s. lat. were addressed by proposing another new combination, G. fischeri for the former G. cichoracearum var. fischeri that differs from G. cichoracearum s. str. in having larger chasmothecia and a well distinguished anamorph, and by proposing a new species, G. sonchicola, that is biologically, phylogenetically and morphologically distinct from G. cichoracearum s. str.     

Molecular phylogeny and evolution of subsection Magnicellulatae (Erysiphaceae: Podosphaera) with special reference to host plants

The subsection Magnicellulatae of the genus Podosphaera section Sphaerotheca belongs to the tribe Cystotheceae of the Erysiphaceae, which has the characteristic of producing catenate conidia with distinct fibrosin bodies. In this study, we newly determined the nucleotide sequences of the D1/D2 domains of the 28S rDNA region and the sequences of the rDNA internal transcribed spacer (ITS) region to investigate the relationships between the phylogeny of this fungal group and their host plants. The results indicated that the 28S rDNA region is too conservative for phylogenetic analysis of this fungal group. The phylogenetic analysis using 95 ITS sequences demonstrated that two or more Magnicellulatae taxa often infect the same plant genus or species. Although there is a close relationship between Magnicellulatae and asteraceous hosts, this association seems to be not as strict as that between Golovinomyces and the Asteraceae. The difference between the two fungal groups may be explained by their different evolutionary timing.     

Molecular phylogeny supports a Northern Hemisphere origin of Golovinomyces (Ascomycota: Erysiphales)

Golovinomyces is a strictly herb-parasitic genus in the Erysiphaceae. Host–parasite co-speciation was reported recently between the genus Golovinomyces and Asteraceae from molecular phylogenetic analyses. The Asteraceae originated in South America and latterly expanded their geographic distribution into the Northern Hemisphere. If the co-speciation between Golovinomyces and Asteraceae originated in South America, the geographic origin of Golovinomyces could be assumed to be South America. To address this question, Golovinomyces species from hosts of the tribe Mutisieae, an asteraceous tribe endemic to South America, were collected and the ITS and 28S rDNA regions sequenced. Results indicate that Oidium mutisiae and Golovinomyces leuceriae isolated from the Mutisieae do not belong at the base of the Golovinomyces tree. Instead, they are situated separately within two different clades of Golovinomyces isolates from the Northern Hemisphere. Therefore, the tribe Mutisieae is not the most early host of Golovinomyces. Present results suggest that Golovinomyces originated in the Northern Hemisphere, and not in South America. The new species Oidium reginae for the previous O. mutisiae on Mutisia decurrens is proposed.     

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.     

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.

     

Rooting Around the Eutherian Family Tree: the Origin and Relations of the Taeniodonta

Placing early groups into the overall phylogeny of eutherian mammals can be challenging, particularly when the group does not have extant members. We investigated the relationships of the Taeniodonta, an extinct group from the Late Cretaceous through Paleogene of North America. This group has a few purported close relatives, including Cimolestes, Procerberus, and Alveugena, that may form a sequence of ancestors and descendants. The leading hypothesis is that Procerberus gave rise to taeniodonts through Alveugena. We test this hypothesis and analyze relations to known stem and crown Eutheria to determine the place of taeniodonts in eutherian phylogeny. Cladistic analyses were performed using previously published characters and datasets, namely a taeniodont/cimolestid specific dataset and a reanalysis of Wible and colleagues (2009), with added taxa for both. Our studies suggest that taeniodonts arose from Cimolestes through Alveugena, that Procerberus is more distantly related to taeniodonts, and that taeniodonts and their relatives are stem eutherians. We diagnose the Taeniodonta based on these analyses. Other Paleogene groups, especially those allied with Cimolestes such as tillodonts and pantolestans, merit further study. Our findings indicate that stem eutherians such as the Taeniodonta, in addition to crown eutherians, continued to diversify during the Paleogene.     

Erysiphe kenjiana (Erysiphales), a new invasive fungus in Europe

An Asian powdery mildew fungus Erysiphe (Uncinula) kenjiana (Erysiphales, Ascomycota) has been found in Ukraine. This is the first record of this fungus in Europe. In 2007, E. kenjiana was collected on four Ulmus species in Kiev. All locations adjoined railways or an airport. Development of E. kenjiana was epiphytotic. This species was not found on elms surveyed at towns situated north-east, east or south of Kiev. The fungus may have been brought directly to Ukraine by rail or air transport. In 2008, the fungus was also collected in Chernihiv situated north-east of Kiev. It is likely that E. kenjiana will spread over all Ukraine and into countries of central and western Europe in 2009 or later. Molecular phylogenetic analyses using D1/D2 domains of the 28S rDNA and ITS sequences revealed that the Ulmaceae-Cannabaceae-parasitic powdery mildews, including E. kenjiana, form a clade with strong supports, suggesting that these species diverged from a single ancestor and expanded their host ranges within the Ulmaceae and allied Cannabaceae. This hypothesis is supported by these species sharing the unique morphology of enlarged apices on their chasmothecial appendages. These fungi formed part of a larger grouping with species on Fagaceae, Nothofagaceae, Rosaceae, and Sapindaceae with strong statistical supports. These results suggest that Uncinula-like powdery mildew fungi on these plant families exhibit close evolutionary relationships with their hosts.     

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.     

First records of the powdery mildews <Emphasis Type="Italic">Erysiphe platani</Emphasis> and <Emphasis Type="Italic">E. alphitoides</Emphasis> on <Emphasis Type="Italic">Ailanthus altissima</Emphasis> reveal host jumps independent of host phylogeny

The tree-of-heaven Ailanthus altissima (family Simaroubaceae, order Sapindales) is one of the most invasive neophytes in Europe. The tree originated in China and became invasive worldwide in areas with Mediterranean to temperate climates. As known from other invasive plants, only a few pathogens have been reported from A. altissima in Europe, and, to date, powdery mildews on it have been unknown in the European region. Recently, two powdery mildews were found on A. altissima during a survey of neomycetes on non-native plants in Switzerland. Because they did not fit with any of the species known to occur on Simaroubaceae in Asia, they were identified by DNA barcoding using sequences of the ITS region of the n-rDNA, revealing them to be the powdery mildews of plane and oak trees, Erysiphe platani and E. alphitoides. This is the first record of E. platani on a host outside the genus Platanus and its family Platanaceae, as well as its order Proteales. In contrast, E. alphitoides has been reported to occur on several host families and orders. Host jumps over great phylogenetic distances—such as across plant families and orders—appear to be quite common in biogeographically novel associations between Erysiphales species and plants. The consequences of such host jumps for identity and taxonomic placement of species are discussed here. It is further questioned whether both pathogens are usable as biological control agents against the tree-of-heaven.     

Diversity and species boundaries in floricolous downy mildews

Floricolous downy mildews are a monophyletic group of members of the genus Peronospora (Oomycota, Peronosporales). These downy mildews can be found on a variety of families of the Asteridae, including Asteraceae, Campanulaceae, Dipsacaceae, Lamiaceae, and Orobanchaceae. With the exception of Peronospora radii, which can also cause economically relevant losses, sporulation usually takes place only on floral parts of their hosts. However, only very few specimens of these mostly inconspicuous downy mildews have so far been included in molecular phylogenies. Focusing on Lamiaceae, we have investigated multiple specimens of floricolous downy mildews for elucidating species boundaries and host specificity in this group. Based on both mitochondrial and nuclear loci, it became apparent that phylogenetic lineages in the Lamiaceae seem to be host genus specific and significant sequence diversity could be found between lineages. Based on distinctiveness in both phylogenetic reconstructions and morphology, the downy mildew on flowers of Stachys palustris is introduced as a new species, Peronospora jagei sp. nov., which can be morphologically distinguished from Peronospora stigmaticola by broader and shorter conidiospores. The diversity of the floricolous down mildews might be higher than previously assumed, although specimens from a much broader set of samples will be needed to confirm this view.     

A new species of Phoenicopsis (Leptostrobales) from the Maastrichtian–Danian of Chukotka,Russia

A new species, Phoenicopsis anadyrensis Nosova, is described based on the leaf morphology and cuticle features from the Maastrichtian–Danian Rarytkin Formation, Chukotka, North-East of Russia. It is characterized by hypostomatic leaves with stomatal bands on the abaxial side, undulate anticlinal epidermal cell walls and papillae on the epidermal cells and on the subsidiary cells of the stomata. The new species is the youngest reliable representative of the genus Phoenicopsis. This record extends the stratigraphic range of Phoenicopsis from its previously known latest records in the early Campanian up to Maastrichtian–Danian. The persistence of the genus Phoenicopsis up to the Cretaceous–Paleogene boundary is most likely related with vicinity to mountain floras associated with Late Cretaceous and Paleogene volcanic uplands.     

The Transition from a Phytopathogenic Smut Ancestor to an Anamorphic Biocontrol Agent Deciphered by Comparative Whole-Genome Analysis

Pseudozyma flocculosa is related to the model plant pathogen Ustilago maydis yet is not a phytopathogen but rather a biocontrol agent of powdery mildews; this relationship makes it unique for the study of the evolution of plant pathogenicity factors. The P. flocculosa genome of ∼23 Mb includes 6877 predicted protein coding genes. Genome features, including hallmarks of pathogenicity, are very similar in P. flocculosa and U. maydis, Sporisorium reilianum, and Ustilago hordei. Furthermore, P. flocculosa, a strict anamorph, revealed conserved and seemingly intact mating-type and meiosis loci typical of Ustilaginales. By contrast, we observed the loss of a specific subset of candidate secreted effector proteins reported to influence virulence in U. maydis as the singular divergence that could explain its nonpathogenic nature. These results suggest that P. flocculosa could have once been a virulent smut fungus that lost the specific effectors necessary for host compatibility. Interestingly, the biocontrol agent appears to have acquired genes encoding secreted proteins not found in the compared Ustilaginales, including necrosis-inducing-Phytophthora-protein- and Lysin-motif- containing proteins believed to have direct relevance to its lifestyle. The genome sequence should contribute to new insights into the subtle genetic differences that can lead to drastic changes in fungal pathogen lifestyles.     

Cretaceous/Paleogene Floral Turnover in Patagonia: Drop in Diversity,Low Extinction,and a Classopollis Spike

Nearly all data regarding land-plant turnover across the Cretaceous/Paleogene boundary come from western North America, relatively close to the Chicxulub, Mexico impact site. Here, we present a palynological analysis of a section in Patagonia that shows a marked fall in diversity and abundance of nearly all plant groups across the K/Pg interval. Minimum diversity occurs during the earliest Danian, but only a few palynomorphs show true extinctions. The low extinction rate is similar to previous observations from New Zealand. The differing responses between the Southern and Northern hemispheres could be related to the attenuation of damage with increased distance from the impact site, to hemispheric differences in extinction severity, or to both effects. Legacy effects of the terminal Cretaceous event also provide a plausible, partial explanation for the fact that Paleocene and Eocene macrofloras from Patagonia are among the most diverse known globally. Also of great interest, earliest Danian assemblages are dominated by the gymnosperm palynomorphs Classopollis of the extinct Mesozoic conifer family Cheirolepidiaceae. The expansion of Classopollis after the boundary in Patagonia is another example of typically Mesozoic plant lineages surviving into the Cenozoic in southern Gondwanan areas, and this greatly supports previous hypotheses of high latitude southern regions as biodiversity refugia during the end-Cretaceous global crisis.