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The North American fungal pathogen Heterobasidion irregulare is currently distributed in pine and oak stands along 103 km of coastline west of Rome, Italy. This paper reviews and expands
the knowledge on impacts, pathways of introduction and invasion, factors driving the invasion and on the dispersal abilities
of this pathogen in Italy. Further, an...
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... al ., 2008). Only six H. irregulare mating factor alleles were identified in the infested area (D’Amico et al ., 2007), and such a finding is also consistent with an introduction of three heterokaryotic genotypes. As a consequence of the effects of serial bottlenecks, genetic diversity of H. irregulare populations decreases with increasing distance from Castelporziano/Castelfusano, supporting an invasion process starting in Castelporziano and ending in the area south of the Circeo National Park (Garbelotto et al ., 2013). Two add- itional observations support this pattern of invasion: (1) disease foci associated with the exotic pathogen were about one order of magnitude larger in Castelporziano than anywhere else, the smallest being in the Circeo National Park and, (2) the large forest of the Circeo National Park was only infested by H. irregulare in its northern portion, suggesting recent colonization from the north, where Castelporziano is located (Gonthier et al ., 2007, 2012). The finding that Castelporziano is the most likely single site of the original introduction has great relevance because it makes it extremely plausible that H. irregulare may have been introduced into Italy through the movement of infected untreated wood by the military. Besides the obvious worldwide implications for policy- making, this conclusion indicates wood of susceptible hosts should not be moved outside the zone of infestation, unless treated. The co-occurrence of a native and a non-native species sharing similar host preference (pines) and the same infection biology has allowed for comparative observations and experiments aimed at elucidating the relative importance of factors driving the invasion. Heterobasidion irregulare introduced to Italy was reported to grow more rapidly than H. annosum in growth test performed in vitro at temperature ranging from 5 to 30 8 C (Scir ` et al ., 2011). However, when genotypes preselected for the absence of alleles introgressed from either species were compared in terms of growth rate no significant differences were observed, at least at temperatures . 8 8 C (Figure 3), suggesting that pure lineages of the two species perform similarly. Likewise, based on the results of comparative inoculation experiments, pathogenicity levels of pure H. irregulare and H. annosum genotypes are comparable on seedlings or cuttings of several pine species, including Italian stone pine, Scots pine and loblolly pine ( P. taeda L.), suggesting the invasion is not driven by a disproportionate pathogenicity of the non-native fungus on native pine species (Garbelotto et al ., 2010). On the other hand, when inoculated in Scots pine logs, H. irregulare genotypes were shown to be able to colonize a volume of wood significantly larger (on average 5 times larger) than H. annosum genotypes (Giordano et al ., 2014). Furthermore, several metrics (i.e. the number of fruiting bodies and PPI , an index summarizing the amount of surface available for spore production) indicated that saprobic growth was positively correlated with fruiting body production (Giordano et al ., 2014). This may provide an explanation for the observation that spore deposition in the infested area was constantly high for the introduced, but not for the native fungal species (Garbelotto et al ., 2010). The latter alternated periods of high spore deposition with periods of low spore deposition (Garbelotto et al ., 2010). Heterobasidion irregulare is able to colonize pure oak stands that are unavailable to its native sister species (Gonthier et al ., 2012), thus broadening the habitats accessible to the non-native pathogen. Although accurate investigations are needed to exclude oc- currence of disease caused by H. irregulare on oaks, preliminary observations suggest it is present in oak stands only as a saprobe (Gonthier et al ., 2012). Cumulatively, results of observations and experiments suggest that differences in transmission potential, referred to as the pathogen’s ability to be transmitted from an infected to an uninfected host, rather than hyper-susceptibility of native hosts may be driving the invasion of the introduced H. irregulare in Italy. Such a finding has important implications for disease control. The rate of spread of H. irregulare , calculated by dividing the distance between Castelporziano and the furthest infested site by the time elapsed since introduction, has been estimated at 1.3 km year 2 1 (Gonthier et al ., 2007). Since the movement of Italian stone pine wood, including firewood, in the area is very limited, it is unlikely that the invasion may have been mediated by human transport. The estimated spread rate is obviously an underestimation as it does not take into account that a certain amount of time must have been required for establishment of the introduced species, during the so called ‘lag-phase’ of the invasion. However, it should be noted that available habitats (forest stands) are extremely fragmented in the infestation area. The analysis of the current distribution of the pathogen and spatial autocorrelation analyses using genetic data may provide a more useful estimate of the true potential dispersal rate of the pathogen and of the effects on its dispersal caused by habitat ...
Citations
... For plant commensals, the genus Starmerella [52] and Candida magnoliae were uncovered [53]. For plant pathogens, the genus Puccinia [54], Heterobasidion irregulare [55], and Colletotrichum gloeosporioides were identified [56]. For wood-decaying fungi, the genus Coprinopsis [57] and Phlebia tremellosa were identified [58]. ...
A vitamin D receptor (VDR) deficiency leads to the dysbiosis of intestinal bacteria and is associated with various diseases, including cancer, infections, and inflammatory bowel disease. However, the impact of a VDR deficiency on fungi and archaea is unknown. We conditionally deleted the VDR in Paneth cells (VDRΔPC), intestinal epithelial cells (VDRΔIEC), or myeloid cells (VDRΔLyz) in mice and collected feces for shotgun metagenomic sequencing and untargeted metabolomics. We found that fungi were significantly altered in each knockout (KO) group compared to the VDRLoxp control. The VDRΔLyz mice had the most altered fungi species (three depleted and seven enriched), followed by the VDRΔPC mice (six depleted and two enriched), and the VDRΔIEC mice (one depleted and one enriched). The methanogen Methanofollis liminatans was enriched in the VDRΔPC and VDRΔLyz mice and two further archaeal species (Thermococcus piezophilus and Sulfolobus acidocaldarius) were enriched in the VDRΔLyz mice compared to the Loxp group. Significant correlations existed among altered fungi, archaea, bacteria, and viruses in the KO mice. Functional metagenomics showed changes in several biologic functions, including decreased sulfate reduction and increased biosynthesis of cobalamin (vitamin B12) in VDRΔLyz mice relative to VDRLoxp mice. Fecal metabolites were analyzed to examine the involvement of sulfate reduction and other pathways. In conclusion, a VDR deficiency caused the formation of altered fungi and archaea in a tissue- and sex-dependent manner. These results provide a foundation about the impact of a host factor (e.g., VDR deficiency) on fungi and archaea. It opens the door for further studies to determine how mycobiome and cross-kingdom interactions in the microbiome community and metabolites contribute to the risk of certain diseases.
... A relatively recently discovered biological invasion is that of the North American fungal plant pathogen H. irregulare, inadvertently introduced a few The alien invasive forest pathogen Heterobasidion irregulare is replacing the native… miles Southwest of Rome, Italy, by the US army in 1944 (Gonthier et al. 2004;). This root rot agent is now associated with significant mortality of Italian stone pine (Pinus pinea) in pure planted pine stands, in mixed oak-pine natural forests and in urban parks located within and around the city of Rome (D'Amico et al. 2007;Gonthier et al. 2007Gonthier et al. , 2014. The current zone of infestation covers an area approximately 103 km long in a Northwest-Southeast direction along the Mediterranean Sea, West of Rome . ...
Invasions by alien pathogens are a major threat to forest conservation. The North American fungal pathogen of conifers Heterobasidion irregulare , inadvertently introduced in Central Italy in the 1940s, has been spreading causing high mortality of Italian stone pine ( Pinus pinea ). While invading newfound niches, H. irregulare has established itself in the current range of the native congener H. annosum . The aims of this study were to determine whether in time: (I) H. irregulare populations may be increasing in size; (II) H. irregulare may be replacing H. annosum , rather than simply coexisting with it; and, (III) H. annosum may disappear in forests infested by H. irregulare . The presence, abundance and distribution of H. annosum and H. irregulare were assessed through an aerobiological assay replicated ten years apart in a forest in which both species have been coexisting. Replacement index (RI), Markov chains and geometric progressions were used to model the interspecific interaction between the two species and to assess the invasiveness of H. irregulare . Results showed that, in 10 years, the incidence of H. annosum dropped from 39.4 to 6.1%, while that of H. irregulare increased from 57.6 to 81.8%, with the alien pathogen replacing the native species (RI = 84.6%) and spreading at a maximum rate of 139 ha/year. Although our models show that the extinction of H. annosum may be unlikely, the ability of H. irregulare to replace it suggests the alien pathogen may also readily colonize those parts of Europe where H. annosum is more abundant than in Central Italy.
... Pinus pinea are iconic trees in Italy and have been showing a rapid decline in Campania and Lazio regions, due in part to the introduction of other invasive pests, including pine tortoise scale (T. parvicornis), western conifer seed bug (Leptoglossus occidentalis Heidemann) and the North American root rot pathogen of pines Heterobasidion irregulare (Gonthier et al., 2014). The impact on tree health by T. parvicornis may be amplified in combination with these other invasive pests. ...
The EFSA Panel on Plant Health performed a pest categorisation of Toumeyella parvicornis (Cockerell) (Hemiptera: Coccidae) for the EU territory. This species is not included in EU Commission Implementing Regulation 2019/2072. T. parvicornis is a soft-scale insect native to North America and has been introduced to the Caribbean region and the EU. It has been present in Italy since 2014 (Abruzzo, Campania, Lazio, and Apulia regions) and in France since 2021 (Provence-Alpes-Côte d'Azur region) and is under official control. It develops on Pinus spp. (Pinaceae), feeding on the needles and twigs, especially on new growth. It is sexually reproductive, has one or more generations each year (three in southern Italy), and adult females overwinter on the Pinus needles. It has a high fecundity, up to 1,014 eggs per female in Italy, with an average of 199 eggs for the summer generation and 730 for the overwintering generation. The main natural dispersal stage is the first instar, which crawls over the plant or may be dispersed further by wind and animals. The species can be transported over longer distances with plants for planting. Large populations cause yellowing, needle loss, reduction in growth and recruitment, flagging, dieback and tree mortality. It has had a significant impact to P. pinea (stone pine) in Italy and caused a catastrophic decline of P. caribbea var. bahamensis (Caribbean pine) in the Turks and Caicos Islands. Adult and immature T. parvicornis could enter the EU with Pinus plants for planting; however, the import of Pinus from third countries where the scale is found is prohibited. Host availability and climate suitability indicate that most of the EU would be suitable for establishment. Phytosanitary measures are available to inhibit further introductions and slow the spread within the EU. T. parvicornis satisfies all the criteria that are within the remit of EFSA to assess for it to be regarded as a potential Union quarantine pest.
... The forest pathogen has been introduced from North America into Italy through infected wood products and currently causes root rot on Italian stone pine (P. pinea) and Aleppo pine (Pinus halepensis) Gonthier et al., 2004Gonthier et al., , 2014Scirè et al., 2008). The exotic forest pathogen shares a conifer habitat with the indigenous relative H. annosum s.s. ...
In boreal and north temperate forests, about 10%–15% of conifer trees (spruce, pine) cut are rotted and commercially less valuable, largely caused by a single pathogen Heterobasidion annosum s.l. The economic effects of Heterobasidion infection approximate to 1 billion euros in losses yearly in Europe. Despite extensive efforts dedicated to unravel the genetic components involved in the pathogenicity and lifestyles of Heterobasidion pathogens, the molecular mechanisms have not been thoroughly understood. Our understanding and perception of Heterobasidion pathogenesis have recently been facilitated due to novel technological advances using “Omics” technology. The availability of the genome and transcriptome of Heterobasidion has led to the discovery of large groups of small secreted proteins (SSPs) or effector-like proteins. Elucidating the functional role of the individual effectors is, however, a very challenging task. Despite the perceived progress, there are still intractable challenges working with Heterobasidion-conifer pathosystem; the long timescale of the disease, lack of mutant lines, large genome size of the host, no avirulent isolates of the pathogen, and inefficient DNA transformation system are some of the obstacles. In spite of the challenges, there have been novel prospects for advances. Novel biotechnology methods are now available and can be deployed to answer many of the fundamental biological questions in this pathosystem.
... In addition, Italian stone pine (Pinus pinea L.) is located along the western coastline of central Italy is currently challenged by the invasive North American species H. irregulare Garbel. & Otrosina [4,5]. The risk posed by H. irregulare to European forestry is high [6]; therefore, the pathogen is recommended for regulation under the European and Mediterranean Plant Protection Organization (EPPO) A2 list. ...
... Those forest stands are included in areas known to be infested by H. annosum s.l. [3,5]. The study sites in north-west of Italy were typical naturally regenerated, uneven-aged and mixed stands, harboring the relevant tree species in sizeable patches. ...
... The study site of central Italy (La Gallinara Park) was an even-aged plantation included in SCIs, preserving coastal Mediterranean habitats. The four study sites were pre-selected based on information on the Heterobasidion airspora pointing to the presence, in each stand, of the host-associated Heterobasidion species determined in previous studies by using the wood disc exposure method combined with the taxon-specific molecular typing of single spore isolates [4,5,10]. In each site, freshly cut stumps were created during selective thinnings carried out in the frame of the ordinary forest management. ...
The Heterobasidion annosum species complex includes major fungal pathogens of conifers worldwide. State-of-the-art preventative stump treatments with urea or with commercial formulations of the fungal biological control agent Phlebiopsis gigantea (i.e., Rotstop®) may become no longer available or are not approved for use in many areas of Europe infested by the three native Heterobasidion species and by the North American invasive H. irregulare, making the development of new treatments timely. The efficacy of Proradix® (based on Pseudomonas protegens strain DSMZ 13134), the cell-free filtrate (CFF) of the same bacterium, a strain of P. gigantea (MUT 6212) collected in the invasion area of H. irregulare in Italy, Rotstop®, and urea was comparatively investigated on a total of 542 stumps of Abies alba, Picea abies, Pinus pinea, and P. sylvestris in forest stands infested by the host-associated Heterobasidion species. Additionally, 139 logs of P. pinea were also treated. Results support the good performances of Rotstop®, and especially of urea against the native Heterobasidion species on stumps of their preferential hosts and, for the first time, towards the invasive North American H. irregulare on stumps of P. pinea. In some experiments, the effectiveness of Proradix® and of the strain of P. gigantea was weak, whereas the CFF of P. protegens strain DSMZ 13134 performed as a valid alternative to urea and Rotstop®. The mechanism of action of this treatment hinges on antibiosis; therefore, further improvements could be possible by identifying the active molecules and/or by optimizing their production. Generally, the performance of the tested treatments is not correlated with the stump size.
... Małecka et al. [32], Gunulf et al. [33] and Kenigsvalde et al. [34] emphasize the importance of these issues. Much research confirms both the high infectious variability of individual pathogen isolates and variation in the timing of saprotrophic colonization of preserved wood of roots or stumps [13,35]. Sierota et al. [36] described genetic variation among commercial strains and indigenous P. gigantea isolates using the random amplified microsatellite (RAMS) method. ...
... At the same time, the mycelium of H. parviporum on the same substrate grew much more slowly for much of the time during the first five days, but by day 6 elongation rates were similar. Similar values are described by Gonthier et al. [35], when comparing H. annosum and H. irregulare mycelial growth in vitro. The comparison of growth rates between several isolates of both fungi showed that mycelial growth rate of P. gigantea (FI from Rotstop and GB from PgSuspension) is higher, but elongation rates of some isolates of H. parviporum (HP1 and HP3) do not differ significantly from the competitor (Figure 4). ...
This review aims to identify possible causes of differing effectiveness of artificial biological control of Heterobasidion root rot by the saprotrophic fungus Phlebiopsis gigantea. We describe published information in terms of pathogen–competitor relationships and the impact of environmental and genetic factors. We also revisit data from original research performed in recent years at the Forest Research Institute in Poland. We hypothesized that, in many cases, competition in roots and stumps of coniferous trees between the necrotrophic Heterobasidion spp. and the introduced saprotroph, Phlebiopsis gigantea, is affected by growth characteristics and enzymatic activity of the fungi, the characteristics of the wood, and environmental conditions. We concluded that both wood traits and fungal enzymatic activity during wood decay in roots and stumps, and the richness of the fungal biota, may limit biological control of root rot. In addition, we identify the need for research on new formulations and isolates of the fungal competitor, Phlebiopsis gigantea, as well as on approaches for accurately identifying the infectious threat from pathogens.
... The former has also become invasive in the coastal pine stands of central Italy after its introduction from eastern USA in the middle of the nineteenth century [108]. Heterobasidion irregulare hybridizes with local H. annosum and represents a threat for European forest ecosystems [109][110][111]. In addition to the above, Douglas-fir and true firs have also been reported to be susceptible to H. occidentale and H. abietinum in North America and Europe, respectively [6]. ...
Pines are major components of native forests and plantations in Europe, where they have both economic significance and an important ecological role. Diseases of pines are mainly caused by fungal and oomycete pathogens, and can significantly reduce the survival, vigor, and yield of both individual trees and entire stands or plantations. Pine pitch canker (PPC), caused by Fusarium circinatum (Nirenberg and O'Donnell), is among the most devastating pine diseases in the world, and is an example of an emergent invasive disease in Europe. The effects of microbial interactions on plant health, as well as the possible roles plant microbiomes may have in disease expression, have been the focus of several recent studies. Here, we describe the possible effects of co-infection with pathogenic fungi and oomycetes with F. circinatum on the health of pine seedlings and mature plants, in an attempt to expand our understanding of the role that biotic interactions may play in the future of PPC disease in European nurseries and forests. The available information on pine pathogens that are able to co-occur with F. circinatum in Europe is here reviewed and interpreted
... Thanks to this assay, it was also possible to identify H. irregulare for the first time in British Columbia, Canada. There are multiple advantages provided by this new diagnostic method: (1) Current distribution of Heterobasidion in North America can be mapped to the species level; (2) wood for export can be tested specifically for the presence of Heterobasidion; and (3) species-level diagnosis of Heterobasidion may help formulate better disease management strategies. ...
Heterobasidion annosum sensu lato is a species complex of pathogenic white-rot wood decay fungi which cause root and butt rot in conifer and hardwood species across the Northern hemisphere. Annual losses to forest managers are valued in the billions of dollars, due to tree mortality, reduction in timber yield, and wood decay. In North America, H. irregulare and H. occidentale have a partially overlapping host and geographic range, cause similar disease symptoms and produce similar fruiting bodies, making discrimination between the two of them often difficult. We developed two sets of primers that bind specifically to conserved, but species-specific portions of glyceraldehyde 3-phosphate dehydrogenase and elongation factor 1α alleles. The method is sensitive enough to detect either species from infected wood. Analysis of North American isolates has further clarified the distribution of both species on this continent, including the detection of H. irregulare for the first time on ponderosa pine (Pinus ponderosa) and eastern white pine (Pinus strobus) in British Columbia. This method has the potential to be a valuable tool for the detection of the pathogen in exported/imported wood products, as well as for the further identification and assessment of the distribution of North American Heterobasidion species.
... Thanks to this assay, it was also possible to identify H. irregulare for the first time in British Columbia, Canada. There are multiple advantages provided by this new diagnostic method: (1) Current distribution of Heterobasidion in North America can be mapped to the species level; (2) wood for export can be tested specifically for the presence of Heterobasidion; and (3) species-level diagnosis of Heterobasidion may help formulate better disease management strategies. ...
Heterobasidion annosum sensu lato is a species complex of pathogenic white-rot wood decay fungi which cause root and butt rot in conifer and hardwood species across the Northern hemisphere. Annual losses to forest managers are valued in the billions of dollars due to tree mortality, reduction in timber yield, and wood decay. In North America, H. irregulare and H. occidentale have a partially overlapping host and geographic range, cause similar disease symptoms and produce similar fruiting bodies, making discrimination between the two of them often difficult. We developed two sets of primers that bind specifically to conserved but species-specific portions of glyceraldehyde 3-phosphate dehydrogenase and elongation factor 1α alleles. The method is sensitive enough to detect either species from infected wood. Analysis of North American isolates has further clarified the distribution of both species on this continent, including the detection of H. irregulare for the first time on ponderosa pine (Pinus ponderosa) and eastern white pine (Pinus strobus) in British Columbia. This method has the potential to be a valuable tool for the detection of the pathogen in exported/imported wood products, as well as for the further identification and assessment of the distribution of North American Heterobasidion species
... Hence, priority for surveys, detection and eradication of H. irregulare should be given to areas where H. annosum is well established. Because the complete eradication of H. irregulare in the current zone of infestation is unrealistic ( Gonthier et al., 2014), the only possible way to effectively manage the disease is to intercept its expansion by promptly eliminating new outbreaks outside the current zone of infestation. A fast and specific detection method based on Loop-mediated isothermal AMPlification (LAMP) of nuclear markers has been recently developed for H. irregulare and is recommended for that purpose ( Sillo et al., 2018). ...
The North American-introduced fungal plant pathogen Heterobasidion irregulare has become invasive in pine stands of central Italy and has broadly hybridized with the native congeneric species H. annosum. In this study, by genotyping Heterobasidion fruiting bodies and mycelia in pine logs inoculated with both fungal species, we showed that H. irregulare developed fruiting bodies at a 1.9-fold higher frequency when spatially overlapping with H. annosum than when by itself. In spite of different fruiting rates, all fruiting bodies were morphologically identical, independently of where they were formed, indicating that increased fruiting rate is likely to increase production of spores. Although all possible nuclear-mitochondrial combinations were identified in hybrids formed in inoculated pine logs, hybrids with nuclei of both species and the H. irregulare mitochondrion were favoured, while hybrids with both nuclei of one species and mitochondria of the other species were less frequent. Based on these results, predictions on the wider invasion of H. irregulare in Europe and recommendations for its containment are formulated.
