scholarly journals The Parauncinula polyspora Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi

mBio ◽  
2019 ◽  
Vol 10 (5) ◽  
Author(s):  
Lamprinos Frantzeskakis ◽  
Márk Z. Németh ◽  
Mirna Barsoum ◽  
Stefan Kusch ◽  
Levente Kiss ◽  
...  
Keyword(s):  
Powdery Mildew ◽  
Defense Mechanism ◽  
Repetitive Sequences ◽  
Draft Genome ◽  
Model Systems ◽  
Powdery Mildew Fungus ◽  
Evolutionary Trajectory ◽  
Reproduction Strategy ◽  
Powdery Mildew Fungi ◽  
Fungal Genes

ABSTRACT Due to their comparatively small genome size and short generation time, fungi are exquisite model systems to study eukaryotic genome evolution. Powdery mildew fungi present an exceptional case because of their strict host dependency (termed obligate biotrophy) and the atypical size of their genomes (>100 Mb). This size expansion is largely due to the pervasiveness of transposable elements on 70% of the genome and is associated with the loss of multiple conserved ascomycete genes required for a free-living lifestyle. To date, little is known about the mechanisms that drove these changes, and information on ancestral powdery mildew genomes is lacking. We report genome analysis of the early-diverged and exclusively sexually reproducing powdery mildew fungus Parauncinula polyspora, which we performed on the basis of a natural leaf epiphytic metapopulation sample. In contrast to other sequenced species of this taxonomic group, the assembled P. polyspora draft genome is surprisingly small (<30 Mb), has a higher content of conserved ascomycete genes, and is sparsely equipped with transposons (<10%), despite the conserved absence of a common defense mechanism involved in constraining repetitive elements. We speculate that transposable element spread might have been limited by this pathogen’s unique reproduction strategy and host features and further hypothesize that the loss of conserved ascomycete genes may promote the evolutionary isolation and host niche specialization of powdery mildew fungi. Limitations associated with this evolutionary trajectory might have been in part counteracted by the evolution of plastic, transposon-rich genomes and/or the expansion of gene families encoding secreted virulence proteins. IMPORTANCE Powdery mildew fungi are widespread and agronomically relevant phytopathogens causing major yield losses. Their genomes have disproportionately large numbers of mobile genetic elements, and they have experienced a significant loss of highly conserved fungal genes. In order to learn more about the evolutionary history of this fungal group, we explored the genome of an Asian oak tree pathogen, Parauncinula polyspora, a species that diverged early during evolution from the remaining powdery mildew fungi. We found that the P. polyspora draft genome is comparatively compact, has a low number of protein-coding genes, and, despite the absence of a dedicated genome defense system, lacks the massive proliferation of repetitive sequences. Based on these findings, we infer an evolutionary trajectory that shaped the genomes of powdery mildew fungi.

scholarly journals Gene erosion and genome expansion in a group of highly host-specialized fungal phytopathogens

2018 ◽  
Author(s):  
Lamprinos Frantzeskakis ◽  
Márk Z. Németh ◽  
Mirna Barsoum ◽  
Stefan Kusch ◽  
Levente Kiss ◽  
...  
Keyword(s):  
Defense Mechanism ◽  
Gene Families ◽  
Exceptional Case ◽  
Model Systems ◽  
Evolutionary Trajectory ◽  
Virulence Proteins ◽  
Niche Specialization ◽  
Reproduction Strategy ◽  
Fungal Genomes ◽  
Fungal Phytopathogens

Due to their comparatively small genome size and short generation time, fungi are exquisite model systems to study eukaryotic genome evolution. Powdery mildew (PM) fungi present an exceptional case where their strict host dependency (a lifestyle termed obligate biotrophy) is associated with some of the largest fungal genomes sequenced so far (>100 Mbp). This size expansion is largely due to the pervasiveness of transposable elements (TEs), which can cover more than 70% of these genomes, and is associated with the loss of multiple conserved ascomycete genes (CAGs) required for a free-living lifestyle. To date, little is known about the mechanisms that drove this expansion, and information on ancestral PM genomes is lacking. We report the genome analysis of the early-diverged PM species Parauncinula polyspora that in contrast to most other PMs reproduces exclusively sexually. The P. polyspora genome is surprisingly small (<30 Mb) and sparsely equipped with TEs (<10%), despite the conserved absence of a common defense mechanism (RIP) involved in constraining repetitive elements. The genome still harbors the majority of the CAGs that are absent in the genomes of the recently evolved PMs. We speculate that TE spread might have been limited by its unique reproduction strategy and host features and further hypothesize that the loss of CAGs may promote the evolutionary isolation and host niche specialization of PM fungi. Limitations associated with this evolutionary trajectory might have been in part counteracted by the evolution of plastic, TE-rich genomes and/or the expansion of gene families encoding secreted virulence proteins.

Studies of the powdery-mildew fungus, Leveillula taurica, on green pepper. II. Light and electron microscopic observation of the infection process

1979 ◽  
Vol 57 (22) ◽  
pp. 2501-2508 ◽  
Author(s):  
Hitoshi Kunoh ◽  
Mitsuru Kohno ◽  
Sadayoshi Tashiro ◽  
Hiroshi Ishizaki
Keyword(s):  
Powdery Mildew ◽  
Light And Electron Microscopy ◽  
Host Cells ◽  
Outer Cell ◽  
Lipid Bodies ◽  
Powdery Mildew Fungus ◽  
Green Pepper ◽  
Ultrastructural Studies ◽  
Leveillula Taurica ◽  
Powdery Mildew Fungi

Almost all ultrastructural studies of powdery-mildew fungi have been focused on the epiparasitic fungi. In this paper, one of the endoparasitic powdery-mildew fungi, Leveillula taurica (Lev.) Arn., on green pepper (Capsicum annuum L. var. angulosum Mill.) leaves was investigated by light and electron microscopy. Most germinated conidia formed a lobed adhesion body (similar to the appressorium in morphology but different in function) before stomatal invasion. The track of the adhesion body on the leaf epidermis was depressed, and no cuticular perforations were observed in it. After stomatal invasion, infection hyphae grew extensively into the intercellular spaces of the leaves and formed haustoria in the spongy- and palisade-parenchyma cells. The haustorium was flask shaped with a neck arising from the intercellular hypha. The overall profiles of the haustorium resembled those of epiphytic powdery-mildew fungi of other authors; the haustorium was composed of a nucleate central body and many anucleate lobes, and the entire structure was bounded by an extrahaustorial membrane. Papillae consisting of three distinct regions formed against the outer cell walls at the site of penetration. The most obvious alteration in infected host cells was a marked increase in the number of large lipid bodies. Lipid bodies increased in number with time after haustorial formation. They appeared first in the host cytoplasm near the extrahaustorial membrane, then in the extrahaustorial matrix and haustorial body.

scholarly journals The partial duplication of an E3-ligase gene in Triticeae species mediates resistance to powdery mildew fungi

2017 ◽  
Author(s):  
Jeyaraman Rajaraman ◽  
Dimitar Douchkov ◽  
Stefanie Lück ◽  
Götz Hensel ◽  
Daniela Nowara ◽  
...  
Keyword(s):  
Powdery Mildew ◽  
E3 Ligase ◽  
Defense Responses ◽  
Duplication Event ◽  
Stable Gene ◽  
Cellular Functions ◽  
Powdery Mildew Fungus ◽  
Crop Species ◽  
Powdery Mildew Fungi ◽  
Plant Pathogen Interactions

ABSTRACTIn plant-pathogen interactions, components of the plant ubiquitination machinery are preferred targets of pathogen-encoded effectors suppressing defense responses or co-opting host cellular functions for accommodation. Here, we employed transient and stable gene silencing-and over-expression systems in Hordeum vulgare (barley) to study the function of HvARM1 (for H. vulgare Armadillo 1), a partial gene duplicate of the U-box/armadillo-repeat E3 ligase HvPUB15 (for H. vulgare Plant U-Box 15). The partial ARM1 gene was derived from an ancient gene-duplication event in a common ancestor of the Triticeae tribe of grasses comprising the major crop species H. vulgare, Triticum aestivum and Secale cereale. The barley gene HvARM1 contributed to quantitative host as well as nonhost resistance to the biotrophic powdery mildew fungus Blumeria graminis, and allelic variants were found to be associated with powdery mildew-disease severity. Both HvPUB15 and HvARM1 proteins interacted in yeast and plant cells with the susceptibility-related, plastid-localized barley homologs of THF1 (for Thylakoid formation 1) and of ClpS1 (for Clp-protease adaptor S1) of Arabidopsis thaliana. The results suggest a neo-functionalization HvARM1 to increase resistance against powdery mildew and provide a link to plastid function in susceptibility to biotrophic pathogen attack.

scholarly journals Host-Induced Gene Silencing in Barley Powdery Mildew Reveals a Class of Ribonuclease-Like Effectors

2013 ◽  
Vol 26 (6) ◽  
pp. 633-642 ◽  
Author(s):  
Clara Pliego ◽  
Daniela Nowara ◽  
Giulia Bonciani ◽  
Dana M. Gheorghe ◽  
Ruo Xu ◽  
...  
Keyword(s):  
Powdery Mildew ◽  
Gene Silencing ◽  
Transcript Abundance ◽  
Powdery Mildew Fungus ◽  
Host Cell Death ◽  
Barley Powdery Mildew ◽  
Biotrophic Pathogens ◽  
Powdery Mildew Fungi ◽  
Bona Fide ◽  
Do So

Obligate biotrophic pathogens of plants must circumvent or counteract defenses to guarantee accommodation inside the host. To do so, they secrete a variety of effectors that regulate host immunity and facilitate the establishment of pathogen feeding structures called haustoria. The barley powdery mildew fungus Blumeria graminis f. sp. hordei produces a large number of proteins predicted to be secreted from haustoria. Fifty of these Blumeria effector candidates (BEC) were screened by host-induced gene silencing (HIGS), and eight were identified that contribute to infection. One shows similarity to β-1,3 glucosyltransferases, one to metallo-proteases, and two to microbial secreted ribonucleases; the remainder have no similarity to proteins of known function. Transcript abundance of all eight BEC increases dramatically in the early stages of infection and establishment of haustoria, consistent with a role in that process. Complementation analysis using silencing-insensitive synthetic cDNAs demonstrated that the ribonuclease-like BEC 1011 and 1054 are bona fide effectors that function within the plant cell. BEC1011 specifically interferes with pathogen-induced host cell death. Both are part of a gene superfamily unique to the powdery mildew fungi. Structural modeling was consistent, with BEC1054 adopting a ribonuclease-like fold, a scaffold not previously associated with effector function.

scholarly journals Infection of papaya (Carica papaya) by four powdery mildew fungi

2021 ◽  
Vol 60 (1) ◽  
pp. 37-49
Author(s):  
Diána SERESS ◽  
Gábor M. KOVÁCS ◽  
Orsolya MOLNÁR ◽  
Márk Z. NÉMETH
Keyword(s):  
Powdery Mildew ◽  
New Record ◽  
Species Complex ◽  
Carica Papaya ◽  
Phylogenetic Analyses ◽  
Molecular Taxonomy ◽  
Podosphaera Xanthii ◽  
Powdery Mildew Fungus ◽  
Molecular Phylogenetic ◽  
Powdery Mildew Fungi

Papaya (Carica papaya L.) is an important fruit crop in many tropical and subtropical countries. Powdery mildew commonly affects this host, causing premature leaf loss, reduced yields and poor fruit quality. At least fifteen different fungi have been identified as the causal agents of papaya powdery mildew. Powdery mildew symptoms were detected on potted papaya plants growing in two locations in Hungary. This study aimed to identify the causal agents. Morphology of powdery mildew samples was examined, and sequences of two loci were used for molecular taxonomic identifications. Only anamophs were detected in all samples, and four morphological types were distinguished. Most samples had Pseudoidium anamorphs, while some were of the Fibroidium anamorph. Based on morphology and molecular taxonomy, the Fibroidium anamorph  was identified as Podosphaera xanthii. The Pseudoidium anamorphs corresponded to three different Erysiphe species: E. cruciferarum, E. necator and an unidentified Erysiphe sp., for which molecular phylogenetic analyses showed it belonged to an unresolved species complex of E. malvae, E. heraclei and E. betae. Infectivity of P. xanthii and E. necator on papaya was verified with cross inoculations. A review of previous records of powdery mildew fungi infecting papaya is also provided. Podosphaera xanthii was known to infect, and E. cruciferarum was suspected to infect Carica papaya, while E. necator was recorded on this host only once previously. No powdery mildew fungus belonging to the E. malvae/E. heraclei/E. betae species complex is known to infect papaya or any other plants in the Caricaceae, so the unidentified Erysiphe sp. is a new record on papaya and the Caricaceae. This study indicates host range expansion of this powdery mildew fungus onto papaya.

scholarly journals Functional Conservation of Wheat and Rice Mlo Orthologs in Defense Modulation to the Powdery Mildew Fungus

2002 ◽  
Vol 15 (10) ◽  
pp. 1069-1077 ◽  
Author(s):  
Candace Elliott ◽  
Fasong Zhou ◽  
Wolfgang Spielmeyer ◽  
Ralph Panstruga ◽  
Paul Schulze-Lefert
Keyword(s):  
Powdery Mildew ◽  
Defense Mechanism ◽  
Wild Type ◽  
Cell Level ◽  
Powdery Mildew Fungus ◽  
Formae Speciales ◽  
Functional Conservation ◽  
Powdery Mildews ◽  
Basal Defense ◽  
Related Proteins

Homologs of barley Mlo are found in syntenic positions in all three genomes of hexaploid bread wheat, Triticum aestivum, and in rice, Oryza sativa. Candidate wheat orthologs, designated TaMlo-A1, TaMlo-B1, and TaMlo-D1, encode three distinct but highly related proteins that are 88% identical to barley MLO and appear to originate from the three diploid ancestral genomes of wheat. TaMlo-B1 and the rice ortholog, OsMlo2, are able to complement powdery mildew-resistant barley mlo mutants at the single-cell level. Overexpression of TaMlo-B1 or barley Mlo leads to super-susceptibility to the appropriate powdery mildew formae speciales in both wild-type barley and wheat. Surprisingly, overexpression of either Mlo or TaMlo-B1 also mediates enhanced fungal development to tested inappropriate formae speciales. These results underline a regulatory role for MLO and its wheat and rice orthologs in a basal defense mechanism that can interfere with forma specialis resistance to powdery mildews.

Initial events in the colonisation of tomatoes by Oidium lycopersici, a distinct powdery mildew fungus of Lycopersicon species

2000 ◽  
Vol 78 (10) ◽  
pp. 1361-1366 ◽  
Author(s):  
Hannah E Jones ◽  
John M Whipps ◽  
Barry J Thomas ◽  
Tim LW Carver ◽  
Sarah J Gurr
Keyword(s):  
Electron Microscopy ◽  
Scanning Electron Microscopy ◽  
Powdery Mildew ◽  
Intergenic Spacer ◽  
Powdery Mildew Fungus ◽  
Subsequent Formation ◽  
Powdery Mildew Fungi ◽  
Tomato Powdery Mildew ◽  
Oidium Lycopersici ◽  
Scanning Electron

The rDNA intergenic spacer sequence of Oidium lycopersici (ana.; Cooke & Massee 1888, emend. Noordeloos and Loerakker 1989, emend. Mieslerova and Lebeda 1999) was determined and compared with the sequences of other powdery mildews. This pathogen was shown to be distinct from other powdery mildew fungi found on tomato, but it exhibited a close similarity to Erysiphe aquilegiae var. ranunculi. The initial events involved in the germination of conidia and subsequent formation of the appressorium in the newly described powdery mildew of tomato, O. lycopersici, were studied by light and scanning electron microscopy. Scanning electron microscopy revealed the conidial coat to be smooth to slightly rugose and the appressoria to be multilobed and attached to the host by a mucilaginous pad of extracellular material.Key words: Oidium lycopersici, tomato powdery mildew, ITS, life cycle, light microscopy, electron microscopy.

scholarly journals A Hybrid Genome Assembly Resource for Podosphaera xanthii, the Main Causal Agent of Powdery Mildew Disease in Cucurbits

2020 ◽  
Author(s):  
Álvaro Polonio ◽  
Luis Díaz-Martínez ◽  
Dolores Fernández-Ortuño ◽  
Antonio de Vicente ◽  
Diego F. Romero ◽  
...  
Keyword(s):  
Powdery Mildew ◽  
Genome Assembly ◽  
Reference Genome ◽  
Repetitive Sequences ◽  
Causal Agent ◽  
Podosphaera Xanthii ◽  
Reference Genome Assembly ◽  
Long Reads ◽  
Hybrid Genome ◽  
Powdery Mildew Fungi

Podosphaera xanthii is the main causal agent of powdery mildew in cucurbits and, arguably, the most important fungal pathogen of cucurbit crops. Here, we present the first reference genome assembly for P. xanthii. We performed a hybrid genome assembly, using reads from Illumina NextSeq550 and PacBio Sequel S3. The short and long reads were assembled into 1,727 scaffolds with a N50 size of 163,173 bp, resulting in a 142 Mb genome size. The combination of homology-based and ab initio predictions allowed predicting 14,911 complete genes. Repetitive sequences comprised 76.2 % of the genome. Our P. xanthii genome assembly improves considerably the molecular resources for research on P. xanthii−cucurbit interactions and provides new opportunities for further genomics, transcriptomics and evolutionary studies in powdery mildew fungi.

scholarly journals First draft genome assemblies of Pleochaeta shiraiana and Phyllactinia moricola, two tree-parasitic powdery mildew fungi with hemiendophytic mycelia

2021 ◽  
Author(s):  
Stefan Kusch ◽  
Niloofar Vaghefi ◽  
Dr. Susumu Takamatsu ◽  
Shu-Yan Liu ◽  
Mark Z. Nemeth ◽  
...  
Keyword(s):  
Powdery Mildew ◽  
Molecular Basis ◽  
Plant Pathogens ◽  
Draft Genome ◽  
Draft Genome Assembly ◽  
Approaches To Study ◽  
Powdery Mildew Fungi ◽  
Genomics Tools ◽  
Genome Assemblies ◽  
Distinct Phylogenetic Lineage

Powdery mildew fungi (Erysiphaceae) are widespread obligate biotrophic plant pathogens. Thus, applying genetic and omics approaches to study these fungi remains a major challenge, particularly for species with hemiendophytic mycelium. These belong to a distinct phylogenetic lineage within the Erysiphaceae. To date, only a single draft genome assembly is available for this clade, determined in Leveillula taurica. Here, we generated the first draft genome assemblies of Pleochaeta shiraiana and Phyllactinia moricola, two tree-parasitic powdery mildew species with hemiendophytic mycelium, representing two genera that have not been investigated with genomics tools yet. Together with the draft genome of L. taurica, these resources will be pivotal for understanding the molecular basis of the lifestyle of these fungi, which is unique within the Erysiphaceae.

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