Worldwide Genetic Structure Elucidates the Eurasian Origin and Invasion Pathways of Dothistroma septosporum, Causal Agent of Dothistroma Needle Blight

Abstract

Dothistroma septosporum, the primary causal agent of Dothistroma needle blight, is one of the most significant foliar pathogens of pine worldwide. Its wide host and environmental ranges have led to its global success as a pathogen and severe economic damage to pine forests in many regions. This comprehensive global population study elucidated the historical migration pathways of the pathogen to reveal the Eurasian origin of the fungus. When over 3800 isolates were examined, three major population clusters were revealed: North America, Western Europe, and Eastern Europe, with distinct subclusters in the highly diverse Eastern European cluster. Modeling of historical scenarios using approximate Bayesian computation revealed the North American cluster was derived from an ancestral population in Eurasia. The Northeastern European subcluster was shown to be ancestral to all other European clusters and subclusters. The Turkish subcluster diverged first, followed by the Central European subcluster, then the Western European cluster, which has subsequently spread to much of the Southern Hemisphere. All clusters and subclusters contained both mating-types of the fungus, indicating the potential for sexual reproduction, although asexual reproduction remained the primary mode of reproduction. The study strongly suggests the native range of D. septosporum to be in Eastern Europe (i.e., the Baltic and Western Russia) and Western Asia.

Seasonal Dynamics of Fungi Associated with Healthy and Diseased Pinus sylvestris Needles in Northern Europe

“…The fungal community composition did not differ between DNB-symptomatic and DNB-free P. sylvestris needles. This provides support to the hypothesis that D. septosporum has been co-evolving a long time with P. sylvestris and its associated mycobiota [ 69 , 70 ].…”

Rapid Detection of Pine Pathogens Lecanosticta acicola, Dothistroma pini and D. septosporum on Needles by Probe-Based LAMP Assays

“…However, many other biotic, abiotic and anthropogenic factors could be important drivers for needle blights epidemics. Among these, the movement of infected planting material between regions and countries is thought to be the main anthropogenic pathway of L. acicola, D. pini and D. septosporum [28][29][30][31].…”

Molecular-Based Reappraisal of a Historical Record of Dothistroma Needle Blight in the Centre of the Mediterranean Region

“…The scientific debate on the geographic origin of D. septosporum is long and not without controversy [13,[49][50][51][52], partly due to the lack of sufficient sampling of the fungus in some regions of its current range. Recently, a large body of work using microsatellite markers for genotyping an unprecedented number of samples collected from across the worldwide range of D. septosporum has indicated Eastern Europe (i.e., the Baltics and Western Russia) and Western Asia as the possible area of origin of the fungus, and hypothesized a possible derivation of Turkish populations from ancestral populations through an ancient separation dating prior to the colonization of Central Europe [53]. In the study by Mullet and colleagues [53], not enough isolates of the fungus from the outbreak in the Sila Massif were included to attempt reconstructing the evolutionary history of that population, while the finding of D. septosporum in the areas of the present study was yet to be confirmed.…”

“…In Corsica, to the best of our knowledge, there is only one published record of DNB, i.e., a single isolate of D. septosporum from P. nigra subsp. laricio included in [53], which has not been transposed yet into the EPPO database (https://gd.eppo.int/taxon/SCIRPI/distribution, accessed on 19 July 2021). According to EPPO, the pathogen was absent from Corsica at least until 2011, when a monitoring campaign was conducted, and no subsequent updates have been reported.…”