Summary
Chestnut blight, caused by Cryphonectria parasitica, is a devastating disease infecting American and European chestnut trees. The pathogen is native to East Asia and was spread to other ...continents via infected chestnut plants. This review summarizes the current state of research on this pathogen with a special emphasis on its interaction with a hyperparasitic mycovirus that acts as a biological control agent of chestnut blight.
Taxonomy
Cryphonectria parasitica (Murr.) Barr. is a Sordariomycete (ascomycete) fungus in the family Cryphonectriaceae (Order Diaporthales). Closely related species that can also be found on chestnut include Cryphonectria radicalis, Cryphonectria naterciae and Cryphonectria japonica.
Host range
Major hosts are species in the genus Castanea (Family Fagaceae), particularly the American chestnut (C. dentata), the European chestnut (C. sativa), the Chinese chestnut (C. mollissima) and the Japanese chestnut (C. crenata). Minor incidental hosts include oaks (Quercus spp.), maples (Acer spp.), European hornbeam (Carpinus betulus) and American chinkapin (Castanea pumila).
Disease symptoms
Cryphonectria parasitica causes perennial necrotic lesions (so‐called cankers) on the bark of stems and branches of susceptible host trees, eventually leading to wilting of the plant part distal to the infection. Chestnut blight cankers are characterized by the presence of mycelial fans and fruiting bodies of the pathogen. Below the canker the tree may react by producing epicormic shoots. Non‐lethal, superficial or callusing cankers on susceptible host trees are usually associated with mycovirus‐induced hypovirulence.
Disease control
After the introduction of C. parasitica into a new area, eradication efforts by cutting and burning the infected plants/trees have mostly failed. In Europe, the mycovirus Cryphonectria hypovirus 1 (CHV‐1) acts as a successful biological control agent of chestnut blight by causing so‐called hypovirulence. CHV‐1 infects C. parasitica and reduces its parasitic growth and sporulation capacity. Individual cankers can be therapeutically treated with hypovirus‐infected C. parasitica strains. The hypovirus may subsequently spread to untreated cankers and become established in the C. parasitica population. Hypovirulence is present in many chestnut‐growing regions of Europe, either resulting naturally or after biological control treatments. In North America, disease management of chestnut blight is mainly focused on breeding with the goal to backcross the Chinese chestnut's blight resistance into the American chestnut genome.
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BFBNIB, DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UILJ, UKNU, UL, UM, UPUK
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•Emerging diseases caused by pathogens are frequently reported in forests worldwide.•Biological control (BC) is still only rarely applied to tree pathogens.•Specificities of hosts and ...pathogens may account for the difficulties in using BC.•To improve BC of pathogens, we suggest to combinetop-down and bottom-up forces.•BC of pathogens should be integrated with other sustainable management strategies.
Biological control (BC) is defined as the use of living natural enemies, antagonists, or competitors (biological control agents) to control other living organisms. In the second half of the last century, the general interest in BC has increased considerably because greater environmental awareness in society and the implementation of integrated pest management (IPM) strategies have pushed towards the development of environmentally friendly control approaches. However, BC is still only rarely used for pathogens (fungi, bacteria, viruses, nematodes, and phytoplasmas) of forest trees. Here, we present and discuss the biological specificities of both the hosts and the fungal pathogens which may account for this situation. To increase the likelihood of BC success, we suggest a holistic approach involving the use of top-down regulators, competitors and amensalists, all exerting pressure on the pathogen, as well as bottom-up forces helping the host (e.g., endophytes, mycorrhiza). Moreover, BC to mitigate emerging forest diseases should be fully integrated into other sustainable management strategies. Finally, we propose guidelines for developing an efficient BC of emerging fungal pathogens of forest trees.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Invasive microbial species constitute a major threat to biodiversity, agricultural production and human health. Invasions are often dominated by one or a small number of genotypes, yet the underlying ...factors driving invasions are poorly understood. The chestnut blight fungus
first decimated the North American chestnut, and a more recent outbreak threatens European chestnut stands. To unravel the chestnut blight invasion of southeastern Europe, we sequenced 230 genomes of predominantly European strains. Genotypes outside of the invasion zone showed high levels of diversity with evidence for frequent and ongoing recombination. The invasive lineage emerged from the highly diverse European genotype pool rather than a secondary introduction from Asia or North America. The expansion across southeastern Europe was mostly clonal and is dominated by a single mating type, suggesting a fitness advantage of asexual reproduction. Our findings show how an intermediary, highly diverse bridgehead population gave rise to an invasive, largely clonally expanding pathogen.
Biological invasions, resulting from deliberate and unintentional species transfers of insects, fungal and oomycete organisms, are a major consequence of globalization and pose a significant threat ...to biodiversity. Limiting damage by non-indigenous forest pathogens requires an understanding of their current and potential distributions, factors affecting disease spread, and development of appropriate management measures. In this review, we synthesize innate characteristics of invading organisms (notably mating system, reproduction type, and dispersal mechanisms) and key factors of the host population (namely host diversity, host connectivity, and host susceptibility) that govern spread and impact of invasive forest pathogens at various scales post-introduction and establishment. We examine spread dynamics for well-known invasive forest pathogens, Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz, Hosoya, comb. nov., causing ash dieback in Europe, and Cryphonectria parasitica, (Murr.) Barr, causing chestnut blight in both North America and Europe, illustrating the importance of host variability (diversity, connectivity, susceptibility) in their invasion success. While alien pathogen entry has proven difficult to control, and new biological introductions are indeed inevitable, elucidating the key processes underlying host variability is crucial for scientists and managers aimed at developing effective strategies to prevent future movement of organisms and preserve intact ecosystems.
•Five mycoviruses were detected in two native populations of Hymenoscyphus fraxineus.•The overall virus prevalence in the Japanese populations was 11.2%.•All the reported viruses belong to new ...species in their respective genera.•A mitovirus with two genomic forms (linear and circular) was characterized.
The native Japanese population of the fungus Hymenoscyphus fraxineus, the causal agent of ash dieback in Europe, was screened for viruses using a high-throughput sequencing method. Five RNA viruses were detected in 116 fungal isolates sequenced via Illumina RNA-seq platform, with an overall virus prevalence of 11.2%. The viruses were completely sequenced by RNA ligase mediated rapid amplification of cDNA ends (RLM-RACE) followed by Sanger sequencing. The sequences appear to represent new species from three established families (Mito-, Endorna- and Partitiviridae), one recognized genus (Botybirnavirus) and a negative-sense single-stranded RNA virus in the order Bunyavirales from the proposed family “Mybuviridae”. The highest prevalence was found for the mitovirus (7.8%), that had two genomic forms (linear and circular), while the other viruses were detected each in one isolate. Co-infection of a mitovirus and an endornavirus was also observed in one of the infected isolates. Here we describe the molecular characterization of the identified viruses. This study expands the diversity of viruses in H. fraxineus and provides the basis for investigating the virus-mediated control of ash dieback in Europe.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Species of Phytophthora (oomycetes, Stramenopila) are among the major emerging pathogens in forests. In this paper three concrete examples are presented, namely the dieback of the Mediterranean scrub ...in Sardinia due to several Phytophthora species, chestnut ink disease caused by Phytophthora cinnamomi in southern Switzerland, and Sudden Larch Death caused by Phytophthora ramorum in the UK. The specificity of each epidemic will be highlighted and possible options to control these harmful pathogens will be discussed.
Les espèces de Phytophthora (oomycètes, straménopiles) occupent une position de premier plan parmi les agents phytopathogènes émergents en forêt. Dans cet article, trois exemples concrets seront présentés, à savoir le déclin du maquis en Sardaigne dû à l’action de plusieurs espèces de Phytophthora, la maladie de l’encre du châtaignier causée par Phytophthora cinnamomi dans le sud de la Suisse, et la mort subite du mélèze causée par Phytophthora ramorum au Royaume-Uni. La spécificité de chaque épidémie sera discutée, ainsi que les options disponibles pour contrôler ces agents pathogènes particulièrement agressifs.
Phytophthora
species are a cause for concern due to their invasive potential and the damage they can cause in agriculture, forestry, and natural ecosystems worldwide. Since water plays a crucial role ...in their dispersal, stream and river baiting is commonly used to survey risk areas for the presence of quarantine
Phytophthora
species. However, our understanding of the distribution and diversity of
Phytophthora
species in European watercourses remains incomplete. This study investigated the presence and diversity of
Phytophthora
species in Swiss watercourses, with a focus on the highly urbanized Swiss Plateau. Over the period 2012–2016, we sampled 32 watercourses, including major rivers and smaller streams. We isolated
Phytophthora
on selective media and sequenced the internal transcribed spacer region to identify the species. We recovered 241
Phytophthora
isolates, representing 11 species from five major clades.
Phytophthora
clade 6 prevailed, with
P. lacustris
being the most common, found in 94.7% of the watercourses. The number of
Phytophthora
species per watercourse ranged from one to five, with no correlation to watercourse complexity. Our study reveals the presence of six previously unreported species in Switzerland, while known invasive species were not found. Watercourses appear less suited to detect invasive pathogenic
Phytophthora
species with a still limited distribution in the environment.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Forest and agroecosystems, as well as animal and human health, are threatened by emerging pathogens. Following decimation of chestnuts in the United States, the fungal pathogen
Cryphonectria ...parasitica
colonized Europe. After establishment, the pathogen population gave rise to a highly successful lineage that spread rapidly across the continent. Core to our understanding of what makes a successful pathogen is the genetic repertoire enabling the colonization and exploitation of host species. Here, we have assembled >100 genomes across two related genera to identify key genomic determinants leading to the emergence of chestnut blight. We found subtle yet highly specific changes in the transition from saprotrophy to latent pathogenicity mostly determined by enzymes involved in carbohydrate metabolism. Large-scale genomic analyses of genes underlying key nutrition modes can facilitate the detection of species with the potential to emerge as pathogens.
ABSTRACT
Emerging fungal pathogens are a threat to forest and agroecosystems, as well as animal and human health. How pathogens evolve from nonpathogenic ancestors is still poorly understood, making the prediction of future outbreaks challenging. Most pathogens have evolved lifestyle adaptations, which were enabled by specific changes in the gene content of the species. Hence, understanding transitions in the functions encoded by genomes gives valuable insight into the evolution of pathogenicity. Here, we studied lifestyle evolution in the genus
Cryphonectria
, including the prominent invasive pathogen
Cryphonectria parasitica
, the causal agent of chestnut blight on
Castanea
species. We assembled and compared the genomes of pathogenic and putatively nonpathogenic
Cryphonectria
species, as well as sister group pathogens in the family Cryphonectriaceae (Diaporthales, Ascomycetes), to investigate the evolution of genome size and gene content. We found a striking loss of genes associated with carbohydrate metabolism (CAZymes) in
C. parasitica
compared to other Cryphonectriaceae. Despite substantial CAZyme gene loss, experimental data suggest that
C. parasitica
has retained wood colonization abilities shared with other
Cryphonectria
species. Putative effectors substantially varied in number, cysteine content, and protein length among species. In contrast, secondary metabolite gene clusters show a high degree of conservation within the genus. Overall, our results underpin the recent lifestyle transition of
C. parasitica
toward a more pathogenic lifestyle. Our findings suggest that a CAZyme loss may have promoted pathogenicity of
C. parasitica
on
Castanea
species. Analyzing gene complements underlying key nutrition modes can facilitate the detection of species with the potential to emerge as pathogens.
IMPORTANCE
Forest and agroecosystems, as well as animal and human health, are threatened by emerging pathogens. Following decimation of chestnuts in the United States, the fungal pathogen
Cryphonectria parasitica
colonized Europe. After establishment, the pathogen population gave rise to a highly successful lineage that spread rapidly across the continent. Core to our understanding of what makes a successful pathogen is the genetic repertoire enabling the colonization and exploitation of host species. Here, we have assembled >100 genomes across two related genera to identify key genomic determinants leading to the emergence of chestnut blight. We found subtle yet highly specific changes in the transition from saprotrophy to latent pathogenicity mostly determined by enzymes involved in carbohydrate metabolism. Large-scale genomic analyses of genes underlying key nutrition modes can facilitate the detection of species with the potential to emerge as pathogens.
global trade in living plants and plant material has significantly increased the geographic distribution of many plant pathogens. As a consequence, several pathogens have been first found and ...described in their introduced range where they may cause severe damage on naïve host species. Knowing the center of origin and the pathways of spread of a pathogen is of importance for several reasons, including identifying natural enemies and reducing further spread. Several Phytophthora species are well-known invasive pathogens of natural ecosystems, including Phytophthora multivora. Following the description of P. multivora from dying native vegetation in Australia in 2009, the species was subsequently found to be common in South Africa where it does not cause any remarkable disease. There are now reports of P. multivora from many other countries worldwide, but not as a commonly encountered species in natural environments.
a global collection of 335 isolates from North America, Europe, Africa, Australia, the Canary Islands, and New Zealand was used to unravel the worldwide invasion history of P. multivora, using 10 microsatellite markers for all isolates and sequence data from five loci from 94 representative isolates. Our population genetic analysis revealed an extremely low heterozygosity, significant non-random association of loci and substantial genotypic diversity suggesting the spread of P. multivora readily by both asexual and sexual propagules. The P. multivora populations in South Africa, Australia, and New Zealand show the most complex genetic structure, are well established and evolutionary older than those in Europe, North America and the Canary Islands.
according to the conducted analyses, the world invasion of P. multivora most likely commenced from South Africa, which can be considered the center of origin of the species. The pathogen was then introduced to Australia, which acted as bridgehead population for Europe and North America. Our study highlights a complex global invasion pattern of P. multivora, including both direct introductions from the native population and secondary spread/introductions from bridgehead populations.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Intraspecific cryptic invasions may occur when new strains of an invasive species are introduced into an area where this species had already been introduced previously. In plant pathogens, such ...invasions are not well studied, even if, potentially, they can have severe consequences. Here, we investigated the effects of a potential intraspecific invasion in Europe of
, the causal agent of chestnut blight. Specifically, we tested the hypotheses that (i) non-European strains are more virulent on
than those already present in Europe because they have never encountered this new host, and (ii) the variation in virulence among strains is higher within native than within introduced populations. In a greenhouse, 2-year-old
seedlings were inoculated with
strains from South Korea, the United States, and Switzerland, and lesion development and seedling mortality were recorded weekly. Additionally, growth and sporulation of the strains were measured in vitro on agar medium at 15 and 24°C. Although lesion growth was similar for all strains, seedlings inoculated with strains from South Korea and Switzerland died faster than seedlings inoculated with strains from the United States. Moreover, in vitro strains from South Korea grew faster and produced more spores at both temperatures than the strains from the other two countries. In conclusion, our results did not support the two hypotheses. All strains, regardless of their origin, were found to be highly virulent on the inoculated chestnut seedlings. Nevertheless, current phytosanitary measures to avoid the introduction of new genotypes of
into Europe should be further implemented.