Search

Invasive forest pathogens can harm cultural, economic, and ecological resources. Here, we demonstrate the potential of endemic tree pathogen resistance in forest disease management using

International audience; Poplar cultivation is an example of highly artificialized and intensive woody plant production (clonal and evenaged cultivation) that resembles crop production more than it does forest production. Since the 19th century, breeders have created poplar varieties, especially interspecific hybrids selected on the basis of agronomic criteria (speed of growth, wood volume, straightness of stem, quality of wood). Because of the compromise between growth and resistance classically described for plants, the poplar cultivars have become a target of choice for many diseases (bacterial canker, scab, leaf blight, rust, Dothichiza, viral disease, etc.) and pests (borer, Saperda, wooly aphid, hornet moth, weevil, etc.). European poplar cultivation experienced several health crises in the 20th century that led breeders to select new varieties on the criterion of resistance to the main diseases. As a result, there were periods of massive use of certain varieties endowed with satisfactory resistance to a disease that were subsequently gradually abandoned as it became apparent that they were too susceptible to another emerging or re-emerging disease. In the particular case of poplar rust caused by the fungus Melampsora larici-populina, we have documented the existence of cycles in the use of certain varieties resistant to rust. Because the fungus is able to circumvent qualitative poplar resistance, a number of wholly resistant varieties became susceptible after just a few years of cultivation. We have shown that the implementation on a regional scale of certain poplar varieties that carry qualitative resistances had structured the M. larici-populina populations on the scale of France. In this way, the varietal distribution of poplar trees has influenced pathogen distribution. These feedback loops between host populations (poplar stands) and pathogen populations are similar to models of host/pathogen co-evolution with an “arms race” between the poplar tree (via breeders and poplar tree farmers) and the pathogens.

Host–parasite systems provide convincing examples of Red Queen co-evolutionary dynamics. Yet, a key process underscored in Van Valen's theory – that arms race dynamics can result in extinction – has never been documented. One reason for this may be that most sampling designs lack the breadth needed to illuminate the rapid pace of adaptation by pathogen populations. In this study, we used a 25-year temporal sampling to decipher the demographic history of a plant pathogen: the poplar rust fungus, Melampsora larici-populina. A major adaptive event occurred in 1994 with the breakdown of R7 resistance carried by several poplar cultivars widely planted in Western Europe since 1982. The corresponding virulence rapidly spread in M. larici-populina populations and nearly reached fixation in northern France, even on susceptible hosts. Using both temporal records of virulence profiles and temporal population genetic data, our analyses revealed that (i) R7 resistance breakdown resulted in the emergence of a unique and homogeneous genetic group, the so-called cultivated population, which predominated in northern France for about 20 years, (ii) selection for Vir7 individuals brought with it multiple other virulence types via hitchhiking, resulting in an overall increase in the population-wide number of virulence types and (iii) – above all – the emergence of the cultivated population superseded the initial population which predominated at the same place before R7 resistance breakdown. Our temporal analysis illustrates how antagonistic co-evolution can lead to population extinction and replacement, hence providing direct evidence for the escalation process which is at the core of Red Queen dynamics.

Key message Increasing human impacts on forests, including unintentional movement of pathogens, climate change, and large-scale intensive plantations, are associated with an unprecedented rate of new diseases. An evolutionary ecology perspective can help address these challenges and provide direction for sustainable forest management. Context Forest pathology has historically relied on an ecological approach to understand and address the practical management of forest diseases. A widening of this perspective to include evolutionary considerations has been increasingly developed in response to the rising rates of genetic change in both pathogen populations and tree populations due to human activities. Aims Here, five topics for which the evolutionary perspective is especially relevant are highlighted. Results The first relates to the evolutionary diversity of fungi and fungal-like organisms, with issues linked to the identification of species and their ecological niches. The second theme deals with the evolutionary processes that allow forest pathogens to adapt to new hosts after introductions or to become more virulent in homogeneous plantations. The third theme presents issues linked to disease resistance in tree breeding programs (e.g., growth-defense trade-offs) and proposes new criteria and methods for more durable resistance. The last two themes are dedicated to the biotic environment of the tree–pathogen system, namely, hyperparasites and tree microbiota, as possible solutions for health management. Conclusion We conclude by highlighting three major conceptual advances brought by evolutionary biology, i.e., that (i) “not everything is everywhere”, (ii) evolution of pathogen populations can occur on short time scales, and (iii) the tree is a multitrophic community. We further translate these into a framework for immediate policy recommendations and future directions for research.

The genetic consequences of range expansions have generally been investigated at wide geographical and temporal scales, long after the colonization event. A unique ecological system enabled us to both monitor the colonization dynamics and decipher the genetic footprints of expansion over a very short time period. Each year an epidemic of the poplar rust (Melampsora larici‐populina) expands clonally and linearly along the Durance River, in the Alps. The colonization dynamics observed in 2004 showed two phases with different genetic outcomes. Upstream, fast colonization maintained high genetic diversity. Downstream, the colonization wave progressively faltered, diversity eroded, and differentiation increased, as expected under recurrent founder events. In line with the high dispersal abilities of rust pathogens, we provide evidence for leapfrog dispersal of clones. Our results thus emphasize the importance of colonization dynamics in shaping spatial genetic structure in the face of high gene flow.

Emergent diseases are an ever-increasing threat to forests and forest ecosystems and necessitate the development of research tools for species that often may have few pre-existing resources. We sequenced the mRNA expressed by the sudden oak death pathogen Phytophthora ramorum and its most susceptible forest host, tanoak, within the same tissue at two time points after inoculation, and in uninfected tanoak controls. Using the P. ramorum genome to differentiate host and pathogen transcripts, we detected more than 850 P. ramorum transcripts at 5 days post-inoculation and a concurrent upregulation of host genes usually associated with pathogenicity. At 1 day, in contrast, we did not detect pathogen expression or significant enrichment of functional categories of host transcripts relative to controls, highlighting the importance of sequencing depth for in planta studies of host-pathogen interactions. This study highlights processes in molecular host-pathogen interactions in forest trees and provides a first reference transcriptome for tanoak, allowing the preliminary identification of disease-related genes in this study and facilitating future work for this and other members of the family Fagaceae.

Aspen (Populus tremuloides) is a temperate North American tree species with a geographical distribution more extensive than any other tree species on the continent. Because it is economically important for pulp and paper industries and ecologically important for its role as a foundation species in forest ecosystems, the decline of aspen in large portions of its range is of serious concern. The availability and annotation of the black cottonwood (Populus trichocarpa) genome enables a range of high throughput sequencing approaches that can be used to understand rangewide patterns of genetic variation, adaptation, and responses to environmental challenges in other Populus species, including aspen. Gene expression studies are particularly useful for understanding the molecular basis of ecological responses, but are limited by the availability of transcriptome data. We explored the aspen transcriptome through the use of high-throughput sequencing with two main goals: (1) characterization of the expressed portion of the P. tremuloides genome in leaves and (2) assessment of variation in gene expression among genets collected from distinct latitudes but reared in a common garden. We also report a large single nucleotide polymorphism dataset that provides the groundwork for future studies of aspen evolution and ecology, and we identify a set of differentially expressed genes across individuals and population boundaries for the leaf transcriptome of P. tremuloides.