Migration patterns and changes in population biology associated with the worldwide spread of the oilseed rape pathogen Leptosphaeria maculans

Abstract

Pathogen introductions into novel areas can lead to the emergence of new fungal diseases of plants. Understanding the origin, introduction pathways, possible changes in reproductive system and population size of fungal pathogens is essential in devising an integrated strategy for the control of these diseases. We used minisatellite markers to infer the worldwide invasion history of the fungal plant pathogen Leptosphaeria maculans, which causes stem canker (blackleg) of oilseed and vegetable brassicas. Clustering analyses partitioned genotypes into distinct populations corresponding to major geographic regions, along with two differentiated populations in Western Canada. Comparison of invasion scenarios using Approximate Bayesian Computation suggested an origin of the pathogen in the USA, the region where epidemics were first recorded, and independent introductions from there over the last few decades into Eastern Canada (Ontario), Europe and Australia. The population in Western Canada appeared to be founded from a source in Ontario and the population in Chile resulted from an admixture between multiple sources. A bottleneck was inferred for the introduction into Western Canada but not into Europe, Ontario or Australia. Clonality appeared high in Western Canada, possibly because environmental conditions there were less conducive to sexual reproduction. Leptosphaeria maculans is a model invasive pathogen with contrasting features in different regions: shallow population structure, high genetic variability and regular sexual recombination in some regions, by comparison with reduced genetic variability, high rates of asexual multiplication, strong population structure or admixture in others.

Genetic Analyses Suggest Separate Introductions of the Pine Pathogen Lecanosticta acicola Into Europe

“…ABC is a statistical framework that calculates the relative probabilities of complex, competing models of evolutionary history of populations and estimates the demographic parameters underlying a given model (Bertorelle et al 2010;Sunnåker et al 2013). This approach can be used to reconstruct the demographic history of invasive species (Boissin et al 2012;Guillemaud et al 2010;Konečný et al 2013), including fungal plant pathogens (Dilmaghani et al 2012;Dutech et al 2012). …”

Population diversity and genomics of the fungal pathogen of canola Leptosphaeria maculans

“…Human transport may aid in transporting infected material to different regions (Travadon et al, 2011). This in turn leads to random mating between isolates from different regions, creating genetic variance at the avirulence loci and assisting the pathogen to overcome host resistance (Dilmaghani et al, 2012).…”

“…A panmictic population is one in which members may reproduce with one another at random (Polk and Peek, 2010). On the other hand, Dilmaghani et al (2012) proposed from minisatellite marker results that two genetically different populations of blackleg are present in Western Canada. Zander et al (2013) conducted a small scale population diversity study using SNPs, whose successful results were used as a foundation for the large-scale study described in Patel et al (2015) (Chapter 3).…”

“…Certain isolates like Lm-16 and Lm-39 also clustered together but were vastly different in the parameters associated with them. It is known that human movement transports and introduces infected seed and plant material from one area to another (Dilmaghani et al, 2012) thereby mixing and changing the population, further attributing to its panmictic nature. The bootstrapping of the phylogenetic tree also supports the theory of a randomly interacting mixed population.…”

“…This sort of adaptive divergence is consistent with the permanent arms race the pathogen is involved in with its host. Previous studies have established that L. maculans possesses a high evolutionary potential and rapidly evolves to overcome host resistance (Chapter 3; Barrins et al, 2004;Rouxel et al, 2011;Travadon et al, 2011;Dilmaghani et al, 2012;Zander et al, 2013;Grandaubert et al, 2014b;Patel et al, 2015). Gene loss via deletion is an effective method of adaptation employed by several fungal pathogens like Magnaporthe oryzae (Couch et al, 2005), Blumeria graminis (Wicker et al, 2013), including L. maculans (Gout et al, 2006b;Fudal et al, 2007).…”