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Re-classification of the causal agent of white grain disorder on wheat as three separate species of Eutiarosporella
Abstract
In the late 1990s, a novel Botryosphaeria-like fungal pathogen was observed causing a disease on wheat in Queensland, characterised as white grain disorder (WGD). In recent years, this disease has sporadically appeared across the eastern states of Australia. In this study, internal transcribed spacer (ITS) region sequences were used to compare these fungi to other Botryosphaeriaceae spp. to show that they should be reclassified as members of the Eutiarosporella genus. Using a small population of WGD isolates, we built a three-loci maximum likelihood tree, using ITS, β-tubulin, and Elongation Factor1-α sequences to show that there are three separate Eutiarosporella spp. found in infected grain. This multigene tree, with the support of phenotypic differences between clades observed in vitro, show that that the causal agents of WGD should be delimited into three divergent species; Eutiarosporella tritici-australis, Eutiarosporella darliae, and Eutiarosporella pseudodarliae.
... In the present study, F. pseudograminearum was isolated up to 3-fold more frequently than F. acuminatum . The wheat pathogenic fungi E. triticiaustralis (Thynne et al. 2015 ) and M. phaseolina (Fouly et al. 1996 ), the causal agents of white grain disorder and charcoal rot, respectively, were only very rarely isolated from wheat roots. ...
Aims
Determine the wheat rhizosphere competence of Trichoderma gamsii strain A5MH and in planta suppression of the Pythium root and Fusarium crown rot pathogens Globisporangium irregulare and Fusarium pseudograminearum.
Methods and results
Wheat was continuously cropped (eight years) at a minimum tillage, low growing season rainfall (GSR ≤ 170 mm) site shown as highly conducive to Pythium root and Fusarium crown rots. Root isolation frequency (RIF) and qPCR were used to determine the rhizosphere dynamics of strain A5MH and the target pathogens at tillering, grain harvest, and in postharvest stubble over the final 2 years. Strain A5MH actively colonized the wheat rhizosphere throughout both growing seasons, had high root abundance at harvest [log 4.5 genome copies (GC) g−1] and persisted in standing stubble for at least 293-d postinoculation. Globisporangium irregulare was most abundant in roots at tillering, whereas F. pseudograminearum was only abundant at harvest and up to 9-fold greater in the drier, second year (GSR 105 mm). Strain A5MH decreased RIF of both pathogens by up to 40%, root abundance of G. irregulare by 100-fold, and F. pseudogaminearum by 700-fold, but was ineffective against crown rot in the second year when pathogen abundance was >log 6.0 GC g−1 root. Strain A5MH increased crop emergence and tillering biomass by up to 40%.
Conclusions
Further trials are required to determine if the A5MH-induced pathogen suppression translates to yield improvements in higher rainfall regions where non-cereal rotations reduce crown rot inoculum.
... Diplodia olivarum was reported on olive, oleaster, carob, grapevine, almond et al.) (Lazzizera et al. 2008;Granata et al. 2011;Linaldeddu et al. 2015;Olmo et al. 2016) or even in very specific hosts (e. g. Eutiarosporella darliae was only reported on infected wheat and wheat-stubble) (Thynne et al. 2015;Farr and Rossman 2021). Different species of Botryosphaeriaceae exhibit different environmental adaptations and host preferences (Braunsdorf et al. 2016). ...
Woody oil plants are important economic trees which are widely cultivated and distributed throughout China. Surveys conducted during 2020 and 2021 on several woody oil plantations from five regions of Sichuan Province, China, revealed a high diversity of Botryosphaerialean fungi. The identification of 50 botryosphaeriaceous isolates was carried out based on both morphology and multi-gene phylogenetic analysis of internal transcribed spacer region (ITS), translation elongation factor 1-alpha gene ( tef1 ) and β-tubulin gene ( tub2 ). This allowed the identification of twelve previously known Botryosphaeriales species: Aplosporella prunicola , A. ginkgonis , Barriopsis tectonae , Botryosphaeria dothidea , Bo. fabicerciana , Diplodia mutila , Di. seriata , Dothiorella sarmentorum , Neofusicoccum parvum , Sardiniella guizhouensis , Sphaeropsis citrigena , and Sp. guizhouensis , and four novel species belonging to the genera Diplodia and Dothiorella , viz. Di. acerigena , Di. pistaciicola , Do. camelliae and Do. zanthoxyli . The dominant species isolated across the surveyed regions were Botryosphaeria dothidea , Sardiniella guizhouensis and Diplodia mutila , representing 20%, 14% and 12% of the total isolates, respectively. In addition, most isolates were obtained from Pistacia chinensis (14 isolates), followed by Camellia oleifera (10 isolates). The present study enhances the understanding of Botryosphaeriales species diversity on woody oil plants in Sichuan Province, China.
... Secondary metabolites, specifically host selective toxins, have been associated with fungal pathogenicity, host range and aggressiveness (Ito et al., 2004;Ohm et al., 2012;Stergiopoulos et al., 2013;Wolpert et al., 2002). In Eutiarosporella spp. that cause white grain disorder (Thynne et al., 2015), the presence of a specific secondary metabolite biosynthetic gene cluster (BGC) allows woody hosts to be infected (Thynne et al., 2019). Secondary metabolite BGCs must consequently also play a role in host range determination in the Botryosphaeriaceae. ...
Next-generation sequencing (NGS) has revolutionized research on fungi including Botryosphaeriaceae, a family of important plant and particularly tree pathogens. This review highlights the impact that NGS-generated genomes and transcriptomes have had on our understanding of the biology and evolution of these fungi. In less than a decade, 49 genomes representing 31 species in eight genera have been published for the Botryosphaeriaceae. These genomes have been used to show that species in this family are capable of sexual reproduction and that the evolution of their mating strategy is highly dynamic, due to multiple independent transitions from a heterothallic ancestral state to homothallism. Comparative genomics has further revealed an abundance of genes involved in infection and aggressiveness. These include plant cell wall-degrading enzymes and secondary metabolite biosynthetic genes as well as genes related to detoxification and cellular transport. Transcriptomics studies have shown that gene expression is tightly regulated and that there are often significant changes in gene expression occurring between early and late infection and as a response to environmental stress. Furthermore, the genomes of species in the Botryosphaeriaceae do not present genomic architecture compartmentalization based on gene and repeat density. Rather, gene organization patterns are influenced by gene co-expression patterns. NGS data have also made possible the development of molecular markers for some species and these can now also be used for species lacking genomic data. The growth of NGS platforms and their integration with other emerging technologies promises an even deeper understanding of the biology and evolution of the Botryosphaeriaceae and other plant pathogens. This will continue to promote and will also revolutionize the field of plant pathology.
This paper represents the fifth One Stop Shop (OSS) series contribution. This series provides background, disease symptoms, pathogen biology and epidemiology (when available) distribution, hosts for the treated genera, and important gene regions for a better resolution. Species that have pathogenic data are also provided under each genus. This fifth OSS paper treats 25 genera of phytopathogenic fungi: Allophoma, Alternaria, Bipolaris, Boeremia, Calonectria, Calophoma, Campylocarpon, Clonastachys, Corynespora, Cryphonectria, Diaporthe, Diplocarpon, Epicoccum, Eutiarosporella, Ganoderma, Hypomyces, Lasiodiplodia, Monilinia, Neocordana, Phragmidium, Pileolaria, Pseudocercospora, Rhynchosporium, Scytalidium and Sphaeropsis.
Sorghum, the fifth-largest cereal crop globally and a C4 crop, mainly grows in arid and semi-arid areas. In 2021-2023, a new foliar disease of sorghum occurred in China. The diseased leaves showed water-soaked symptoms in the leaf tip and margins, resulting in half- and full-leaf desiccation and necrosis, thus affecting plant photosynthesis. A total of 24 Eutiarosporella strains were isolated from symptomatic leaves. Based on morphological characteristics and multi-locus phylogenetic analysis involving ITS, LSU, and EF1-α sequences, and the pathogenicity test, the pathogen of sorghum causing leaf blight in China was identified as Eutiarosporella dactylidis. The virulence of all E. dactylidis strains was evaluated using the spray-mycelium method. Different strains showed significantly different pathogenicities toward a susceptible cultivar, Longza 10, with disease indexes ranging from 23.76 to 60.37. This study first reported leaf blight of sorghum caused by E. dactylidis and named it "Eutiarosporella leaf blight", which provides a theoretical basis for farmers in disease management.
Botryosphaeriales (Dothideomycetes, Ascomycota) occur in a wide range of habitats as endophytes, saprobes, and pathogens. The order Botryosphaeriales has not been subjected to evaluation since 2019 by Phillips and co-authors using phylogenetic and evolutionary analyses. Subsequently, many studies introduced novel taxa into the order and revised several families separately. In addition, no ancestral character studies have been conducted for this order. Therefore, in this study, we re-evaluated the character evolution and taxonomic placements of Botryosphaeriales species based on ancestral character evolution, divergence time estimation, and phylogenetic relationships, including all the novel taxa that have been introduced so far. Maximum likelihood, maximum parsimony, and Bayesian inference analyses were conducted on a combined LSU and ITS sequence alignment. Ancestral state reconstruction was carried out for conidial colour, septation, and nutritional mode. Divergence times estimates revealed that Botryosphaeriales originated around 109 Mya in the early epoch of the Cretaceous period. All six families in Botryosphaeriales evolved in the late epoch of the Cretaceous period (66–100 Mya), during which Angiosperms also appeared, rapidly diversified and became dominant on land. Families of Botryosphaeriales diversified during the Paleogene and Neogene periods in the Cenozoic era. The order comprises the families Aplosporellaceae, Botryosphaeriaceae, Melanopsaceae, Phyllostictaceae, Planistromellaceae and Saccharataceae. Furthermore, current study assessed two hypotheses; the first one being “All Botryosphaeriales species originated as endophytes and then switched into saprobes when their hosts died or into pathogens when their hosts were under stress”; the second hypothesis states that “There is a link between the conidial colour and nutritional mode in botryosphaerialean taxa”. Ancestral state reconstruction and nutritional mode analyses revealed a pathogenic/saprobic nutritional mode as the ancestral character. However, we could not provide strong evidence for the first hypothesis mainly due to the significantly low number of studies reporting the endophytic botryosphaerialean taxa. Results also showed that hyaline and aseptate conidia were ancestral characters in Botryosphaeriales and supported the relationship between conidial pigmentation and the pathogenicity of Botryosphaeriales species.
Fungi are an important and diverse component in various ecosystems. The methods to identify different fungi are an important step in any mycological study. Classical methods of fungal identification, which rely mainly on morphological characteristics and modern use of DNA based molecular techniques, have proven to be very helpful to explore their taxonomic identity. In the present compilation, we provide detailed information on estimates of fungi provided by different mycologistsover time. Along with this, a comprehensive analysis of the importance of classical and molecular methods is also presented. In orderto understand the utility of genus and species specific markers in fungal identification, a polyphasic approach to investigate various fungi is also presented in this paper. An account of the study of various fungi based on culture-based and cultureindependent methods is also provided here to understand the development and significance of both approaches. The available information on classical and modern methods compiled in this study revealed that the DNA based molecular studies are still scant, and more studies are required to achieve the accurate estimation of fungi present on earth.
The classification of micro-organisms has progressed over the years from their physiological and morphological traits to their genetic make-up. The human microbiome, encompassing genomic data for symbiotic micro-organisms within the human body, is comprised of a plethora of microbes including bacteria, fungi, viruses, and archaea. The importance of the diversity within the microbiome has been explored over recent decades both in determining health and in the development of disease. Microbial diversity is determined using a range of methodologies which have adapted over time and how microbial diversity is understood within the microbiome directly relates to the methods used. Human microbiome studies focus on five body sites including the oral and nasal cavities, the gastrointestinal and urogenital tracts, and the skin. Microbial diversity varies across these sites with bacterial composition often site-specific. Diversity within sites is also dependent on external factors including sex, diet, geography, and personality traits. Dysbiosis of the human microbiome is linked to the development of infectious diseases, obesity, diabetes, cancer, and autoimmune diseases. This chapter reviews the current literature on the methods used to characterize diversity within the microbiome, the variation in diversity observed across the microbiome and the impact of microbiome dysregulation on development of disease.
Coelomycete is a general term used for asexual fungi which produce conidia in fruiting bodies: pycnidial, acervular, cupulate, pycnothyria or stromatic conidiomata. The group contains numerous plant pathogenic, saprobic and endophytic species associated with a wide range of hosts. Traditionally, morphological characters and host associations have been used as criteria to identify and classify coelomycetes, and this has resulted in a poor understanding of their generic and species boundaries. DNA based taxonomic studies have provided a better outlook of the phylogenetic and evolutionary trends in coelomycetes. However, the present outcomes represent only a preliminary step towards the understanding of coelomycetes. Many genera have not been revisited since they were first described. The present study revises the classification of the hyaline-spored coelomycetes and provides a modern taxonomic framework based on both morphology and phylogeny. In total, 248 genera were investigated, of which less than 100 are known to have sequence data. Multi-locus sequence data analyses of 28S nrDNA, 18S nrDNA, ITS, RNA polymerase II second largest subunit (rpb2), and part of the translation elongation factor 1-alpha gene (tef1) and β-tubulin (tub2) gene regions were analysed. As a result, three new genera and 23 new species are introduced. In addition, three new links between sexual and asexual genera are provided. There are 138 genera that lack sequence data, and these are treated as Ascomycota, genera incertae sedis. Line drawings and descriptions are provided based on the examination of types and fresh collections and on the literature.
The type species of the genus Tiarosporella, T. paludosa, is epitypified and confirmed as a member of the Botryosphaeriaceae. Based on morphology and DNA sequence data of the large subunit nuclear ribosomal RNA gene (LSU, 28S) and the internal transcribed spacers (ITS) and 5.8S rRNA gene of the nrDNA operon, the genus Tiarosporella is shown to be poly- and paraphyletic. A group of isolates morphologically similar to T. paludosa cluster to the Phacidiaceae (Phacidiales, Leotiomycetes) and we accommodated them in Darkera, a genus associated with needle diseases of conifers, with D. picea introduced as a novel taxon. This new taxon includes isolates occurring on needles of Picea spp. in Europe (Finland, Norway and Switzerland) and differs from D. parca according to a five-locus alignment consisting of ITS, LSU, partial 18S nuclear ribosomal RNA, translation elongation factor 1-alpha and beta-tubulin genes. Four novel genera are introduced for tiarosporella-like fungi, namely Eutiarosporella based on E. tritici on Triticum aestivum from South Africa, Marasasiomyces based on M. karoo on Eriocephalus sp. from South Africa, Mucoharknessia based on M. cortaderiae on Cortaderia selloana from Argentina, and Sakireeta based on S. madreeya on Aristida setacea from India. Together with the genus Botryobambusa, these genera represent a subclade in the Botryosphaeriaceae that is ecologically diverse, occurring on Poaceae, as well as woody hosts, including endophytes, saprobes, and plant pathogens.
Macrophomina phaseolina is one of the most destructive necrotrophic fungal pathogens that infect more than 500 plant species throughout the world. It can grow rapidly in infected plants and subsequently produces a large amount of sclerotia that plugs the vessels, resulting in wilting of the plant.
We sequenced and assembled ~49 Mb into 15 super-scaffolds covering 92.83% of the M. phaseolina genome. We predict 14,249 open reading frames (ORFs) of which 9,934 are validated by the transcriptome. This phytopathogen has an abundance of secreted oxidases, peroxidases, and hydrolytic enzymes for degrading cell wall polysaccharides and lignocelluloses to penetrate into the host tissue. To overcome the host plant defense response, M. phaseolina encodes a significant number of P450s, MFS type membrane transporters, glycosidases, transposases, and secondary metabolites in comparison to all sequenced ascomycete species. A strikingly distinct set of carbohydrate esterases (CE) are present in M. phaseolina, with the CE9 and CE10 families remarkably higher than any other fungi. The phenotypic microarray data indicates that M. phaseolina can adapt to a wide range of osmotic and pH environments. As a broad host range pathogen, M. phaseolina possesses a large number of pathogen-host interaction genes including those for adhesion, signal transduction, cell wall breakdown, purine biosynthesis, and potent mycotoxin patulin.
The M. phaseolina genome provides a framework of the infection process at the cytological and molecular level which uses a diverse arsenal of enzymatic and toxin tools to destroy the host plants. Further understanding of the M. phaseolina genome-based plant-pathogen interactions will be instrumental in designing rational strategies for disease control, essential to ensuring global agricultural crop production and security.
The B trichothecene toxin-producing clade (B clade) of Fusarium includes the etiological agents of Fusarium head blight, crown rot of wheat and barley and stem and ear rot of maize. B clade isolates also have been recovered from several wild and cultivated grasses, including Dactylis glomerata (orchard grass or cock's foot), one of the world's most important forage grasses. Two isolates from the latter host are formally described here as F. dactylidis. Phenotypically F. dactylidis most closely resembles F. ussurianum from the Russian Far East. Both species produce symmetrical sporodochial conidia that are similar in size and curved toward both ends. However, conidia of F. ussurianum typically end in a narrow apical beak while the apical cell of F. dactylidis is acute. Fusarium dactylidis produced nivalenol mycotoxin in planta as well as low but detectable amounts of the estrogenic mycotoxin zearalenone in vitro. Results of a pathogenicity test revealed that F. dactylidis induced mild head blight on wheat.
Copyright © 2014, Mycologia.
The 97-megabase genomic sequence of the nematode Caenorhabditis elegans reveals over 19,000 genes. More than 40 percent of the predicted protein products find significant matches in other organisms.
There is a variety of repeated sequences, both local and dispersed. The distinctive distribution of some repeats and highly
conserved genes provides evidence for a regional organization of the chromosomes.
Botryosphaeriaceae represents an important and diverse family of latent fungal pathogens of woody plants. We address the question of host range of these fungi by sampling leaves and branches of four native South African trees, including Acacia karroo (Fabaceae), Celtis africana (Cannabaceae), Searsia lancea (Anacardiaceae), and Gymnosporia buxifolia (Celastraceae). Two new species of the Botryosphaeriaceae, namely Tiarosporella africana sp. nov. and Aplosporella javeedii sp. nov. were identified, together with five known species, including Neofusicoccum parvum, Neofusicoccum kwambonambiense, Spencermartinsia viticola, Diplodia pseudoseriata, and Botryosphaeria dothidea. Most Botryosphaeriaceae occurred on more than one host. With the exception of S. lancea, which was infected by A. javeedii all the hosts were infected by more than one Botryosphaeriaceae species. Collectively, the results suggest that some intrinsic host factors, possibly combined with local environmental conditions, affect the distribution and co-infectivity of various hosts by the Botryosphaeriaceae. This would counteract the general ability of a species in the Botryosphaeriaceae to infect a broad range of plants. The combination of host and environmental factors might also explain why some Botryosphaeriaceae with apparently broad host ranges, are found on different suites of hosts in different areas of the world.
Botryosphaeria lutea (anamorph Fusicoccum luteum) most easily is distinguished from other Botryosphaeria spp. by a yellow pigment that is formed in young cultures. This fungus has been reported from a number of cultivated hosts in New Zealand and Portugal. During a survey of Botryosphaeria fungi that occur on native Acacia species in Australia, a yellow pigment was observed in some cultures. These isolates were morphologically similar to B. lutea, but the pigment differed slightly from the one formed by authentic B. lutea isolates. Preliminary data also revealed small differences in ITS rDNA sequence data. The aim of this study was to determine whether these small differences were indicative of separate species or merely variations within B. lutea. Anamorph, teleomorph and culture morphology were compared between B. lutea and Acacia isolates from Australia. Sequence data of two other genome regions, namely the β-tubulin and EF1-α gene and intron regions, were combined with ITS rDNA sequence data to determine the phylogenetic relationship between these isolates. Isolates of B. lutea and those from Australian Acacia species were not significantly different in spore morphology. The yellow pigment, however, was much more distinct in cultures of B. lutea than in cultures from Acacia. There were only a few base pair variations in each of the analyzed gene regions, but these variations were fixed in the two groups in all regions. By combining these data it was clear that B. lutea and the isolates from Acacia were distinct species, albeit very closely related. We, therefore, propose the new epithet B. australis for the fungus from Australia. Botryosphaeria australis also was isolated in this study from exotic Sequoiadendron trees in Australia. Re-analyses of GenBank data in this study showed that B. australis also occurs on other native Australian hosts, namely a Banksia sp. and a Eucalyptus sp., as well as a native Protea sp. in South Africa and on Pistachio in Italy. These records from GenBank have been identified previously as B. lutea. The common occurrence of B. australis on a variety of native hosts across Australia suggests that this fungus is native to this area.
Phytopathogens are a global threat to plant agriculture and biodiversity. The genomics era has lead to an exponential rise in comparative gene and genome studies of both economically significant and insignificant microorganisms. In this review we highlight some recent comparisons and discuss how they identify shared genes or genomic regions associated with host virulence. The two major mechanisms of rapid genome adaptation - horizontal gene transfer and hybridisation - are reviewed and we consider how intra-specific pan-genome sequences encode alternative host specificity. We also discuss the power that access to expansive gene databases provides in aiding the study of phytopathogen emergence. These databases can rapidly enable the identification of an unknown pathogen and its origin, as well as genomic adaptations required for emergence.
Copyright © 2015 Elsevier Ltd. All rights reserved.