Phylogeography, origin and population structure of the self-fertile emerging plant pathogen Phytophthora pseudosyringae.

Phytophthora pseudosyringae is a self-fertile pathogen of woody plants, particularly associated with tree species from the genera Fagus, Notholithocarpus, Nothofagus and Quercus, which is found across Europe and in parts of North America and Chile. It can behave as a soil pathogen infecting roots and the stem collar region, as well as an aerial pathogen infecting leaves, twigs and stem barks, causing particular damage in the United Kingdom and western North America. The population structure, migration and potential outcrossing of a worldwide collection of isolates were investigated using genotyping-by-sequencing. Coalescent-based migration analysis revealed that the North American population originated from Europe. Historical gene flow has occurred between the continents in both directions to some extent, yet contemporary migration is overwhelmingly from Europe to North America. Two broad population clusters dominate the global population of the pathogen, with a subgroup derived from one of the main clusters found only in western North America. Index of association and network analyses indicate an influential level of outcrossing has occurred in this preferentially inbreeding, homothallic oomycete. Outcrossing between the two main population clusters has created distinct subgroups of admixed individuals that are, however, less common than the main population clusters. Differences in life history traits between the two main population clusters should be further investigated together with virulence and host range tests to evaluate the risk each population poses to natural environments worldwide.

Host genotype interacts with aerial spore communities and influences the needle mycobiome of Norway spruce.

The factors shaping the composition of the tree mycobiome are still under investigation. We tested the effects of host genotype, site, host phenotypic traits, and air fungal spore communities on the assembly of the fungi inhabiting Norway spruce needles. We used Norway spruce clones and spore traps within the collection sites and characterized both needle and air mycobiome communities by high-throughput sequencing of the ITS2 region. The composition of the needle mycobiome differed between Norway spruce clones, and clones with high genetic similarity had a more similar mycobiome. The needle mycobiome also varied across sites and was associated with the composition of the local air mycobiome and climate. Phenotypic traits such as diameter at breast height or crown health influenced the needle mycobiome to a lesser extent than host genotype and air mycobiome. Altogether, our results suggest that the needle mycobiome is mainly driven by the host genotype in combination with the composition of the local air spore communities. Our work highlights the role of host intraspecific variation in shaping the mycobiome of trees and provides new insights on the ecological processes structuring fungal communities inhabiting woody plants.

Halophytophthora fluviatilis Pathogenicity and Distribution along a Mediterranean-Subalpine Gradient.

Halophytophthora species have been traditionally regarded as brackish water oomycetes; however, recent reports in inland freshwater call for a better understanding of their ecology and possible pathogenicity. We studied the distribution of Halophytophthora fluviatilis in 117 forest streams by metabarcoding river filtrates taken in spring and autumn and by direct isolation from floating leaves. Pathogenicity on six Fagaceae species and Alnus glutinosa was assessed by stem inoculations. The distribution of H. fluviatilis was correlated with high mean annual temperatures (>93.5% of reports in Ta > 12.2 °C) and low precipitation records. H. fluviatilis was therefore widely distributed in forest streams in a warm-dry climate, but it was mostly absent in subalpine streams. H. fluviatilis was primarily detected in autumn with few findings in spring (28.4% vs. 2.7% of streams). H. fluviatilis was able to cause small lesions on some tree species such as Quercus pubescens, Q. suber and A. glutinosa. Our findings suggest that H. fluviatilis may be adapted to warm and dry conditions, and that it does not pose a significant threat to the most common Mediterranean broadleaved trees.

Vegetation type determines spore deposition within a forest-agricultural mosaic landscape.

Predicting fungal community assembly is partly limited by our understanding of the factors driving the composition of deposited spores. We studied the relative contribution of vegetation, geographical distance, seasonality and weather to fungal spore deposition across three vegetation types. Active and passive spore traps were established in agricultural fields, deciduous forests and coniferous forests across a geographic gradient of ∼600 km. Active traps captured the spore community suspended in air, reflecting the potential deposition, whereas passive traps reflected realized deposition. Fungal species were identified by metabarcoding of the ITS2 region. The composition of spore communities captured by passive traps differed more between vegetation types than across regions separated by >100 km, indicating that vegetation type was the strongest driver of composition of deposited spores. By contrast, vegetation contributed less to potential deposition, which followed a seasonal pattern. Within the same site, the spore communities captured by active traps differed from those captured by passive traps. Realized deposition tended to be dominated by spores of species related to vegetation. Temperature was negatively correlated with the fungal species richness of both potential and realized deposition. Our results indicate that vegetation may be able to maintain similar fungal communities across distances, and likely be the driving factor of fungal spore deposition at landscape level.

Genetic Variation Explains Changes in Susceptibility in a Naïve Host Against an Invasive Forest Pathogen: The Case of Alder and the Phytophthora alni Complex.

Predicting whether naïve tree populations have the potential to adapt to exotic pathogens is necessary owing to the increasing rate of invasions. Adaptation may occur as a result of natural selection when heritable variation in terms of susceptibility exists in the naïve population. We searched for signs of selection on black alder (Alnus glutinosa) stands growing on riverbanks invaded by two pathogens differing in aggressiveness, namely, Phytophthora uniformis (PU) and Phytophthora × alni (PA). We compared the survival and heritability measures from 72 families originating from six invaded and uninvaded (naïve) sites by performing in vitro inoculations. The results from the inoculations were used to assess the relative contribution of host genetic variation on natural selection. We found putative signs of natural selection on alder exerted by PU but not by PA. For PU, we found a higher survival in families originating from invaded sites compared with uninvaded sites. The narrow sense heritability of susceptibility to PU of uninvaded populations was significantly higher than to PA. Simulated data supported the role of heritable genetic variation on natural selection and discarded a high aggressiveness of PA decreasing the transmission rate as an alternative hypothesis for a slow natural selection. Our findings expand on previous attempts of using heritability as a predictor for the likelihood of natural adaptation of naïve tree populations to invasive pathogens. Measures of genetic variation can be useful for risk assessment purposes or when managing Phytophthora invasions.

Contrasting distribution patterns between aquatic and terrestrial Phytophthora species along a climatic gradient are linked to functional traits.

Diversity of microbial organisms is linked to global climatic gradients. The genus Phytophthora includes both aquatic and terrestrial plant pathogenic species that display a large variation of functional traits. The extent to which the physical environment (water or soil) modulates the interaction of microorganisms with climate is unknown. Here, we explored the main environmental drivers of diversity and functional trait composition of Phytophthora communities. Communities were obtained by a novel metabarcoding setup based on PacBio sequencing of river filtrates in 96 river sites along a geographical gradient. Species were classified as terrestrial or aquatic based on their phylogenetic clade. Overall, terrestrial and aquatic species showed contrasting patterns of diversity. For terrestrial species, precipitation was a stronger driver than temperature, and diversity and functional diversity decreased with decreasing temperature and precipitation. In cold and dry areas, the dominant species formed resistant structures and had a low optimum temperature. By contrast, for aquatic species, temperature and water chemistry were the strongest drivers, and diversity increased with decreasing temperature and precipitation. Within the same area, environmental filtering affected terrestrial species more strongly than aquatic species (20% versus 3% of the studied communities, respectively). Our results highlight the importance of functional traits and the physical environment in which microorganisms develop their life cycle when predicting their distribution under changing climatic conditions. Temperature and rainfall may be buffered differently by water and soil, and thus pose contrasting constrains to microbial assemblies.

Winter Conditions Correlate with Phytophthora alni Subspecies Distribution in Southern Sweden.

During the last century, the number of forest pathogen invasions has increased substantially. Environmental variables can play a crucial role in determining the establishment of invasive species. The objective of the present work was to determine the correlation between winter climatic conditions and distribution of two subspecies of the invasive forest pathogen Phytophthora alni: P. alni subspp. alni and uniformis killing black alder (Alnus glutinosa) in southern Sweden. It is known from laboratory experiments that P. alni subsp. alni is more pathogenic than P. alni subsp. uniformis, and that P. alni subsp. alni is sensitive to low temperatures and long frost periods. By studying the distribution of these two subspecies at the northern limit of the host species, we could investigate whether winter conditions can affect the geographical distribution of P. alni subsp. alni spreading northward. Sixteen major river systems of southern Sweden were systematically surveyed and isolations were performed from active cankers. The distribution of the two studied subspecies was highly correlated with winter temperature and duration of periods with heavy frost. While P. alni subsp. uniformis covered the whole range of temperatures of the host, P. alni subsp. alni was recovered in areas subjected to milder winter temperatures and shorter frost periods. Our observations suggest that winter conditions can play an important role in limiting P. alni subsp. alni establishment in cold locations, thus affecting the distribution of the different subspecies of P. alni in boreal regions.