Origin and Domestication of the Fungal Wheat Pathogen Mycosphaerella graminicola via Sympatric Speciation

Abstract

The Fertile Crescent represents the center of origin and earliest known place of domestication for many cereal crops. During the transition from wild grasses to domesticated cereals, many host-specialized pathogen species are thought to have emerged. A sister population of the wheat-adapted pathogen Mycosphaerella graminicola was identified on wild grasses collected in northwest Iran. Isolates of this wild grass pathogen from 5 locations in Iran were compared with 123 M. graminicola isolates from the Middle East, Europe, and North America. DNA sequencing revealed a close phylogenetic relationship between the pathogen populations. To reconstruct the evolutionary history of M. graminicola, we sequenced 6 nuclear loci encompassing 464 polymorphic sites. Coalescence analyses indicated a relatively recent origin of M. graminicola, coinciding with the known domestication of wheat in the Fertile Crescent around 8,000-9,000 BC. The sympatric divergence of populations was accompanied by strong genetic differentiation. At the present time, no genetic exchange occurs between pathogen populations on wheat and wild grasses although we found evidence that gene flow may have occurred since genetic differentiation of the populations.

Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species

“…This genome-wide pattern of genetic variation within a species is very different from that found within other closely related Zymoseptoria species and in other fungal species where genome-wide variation has been described at the population level (13). Z. pseudotritici and Z. tritici diverged recently in the Fertile Crescent during the initiation of agriculture and the domestication of wheat (14). Whereas Z. tritici is specialized onto wheat and has spread globally with its host, Z. pseudotritici is found on a range of very different grass species at the center of origin of the Zymoseptoria species in the Middle East.…”

Diversity, phenology and distribution of Termitomyces species in Côte d’Ivoire

“…Several studies across taxa have shown that the centres of origin are often centres of the genetic diversity (e.g. Banke and McDonald 2005; Stukenbrock et al 2007; for plant pathogens; Moran et al 2003; for reef fishes). The centre of origin of termite fungiculture, under this hypothesis, would then be the centre of higher diversity of both fungus-growing termites and Termitomyces .…”

Best Practices for Population Genetic Analyses

“…Markers with high mutation rates such as microsatellites (also known as simple sequence repeats or SSRs) provide insights into recent divergence (Atallah et al 2010;Baumgartner et al 2010;Berbegal et al 2013;Dunn et al 2014;Dutech et al 2010;Goss et al 2009b), whereas mitochondrial, nuclear or other sequence loci provide inferences about the more distant evolutionary history given the slower mutation rates Goss et al 2009a;Malvarez et al 2007;Schoebel et al 2014;Stukenbrock et al 2007).…”

“…For many reasons, population genetics is a tremendously useful discipline with a long history of application to plant pathology. For example, one can establish where the likely center of origin of a plant pathogen is located, which in turn allows harnessing of plant resistance genes (Goss et al 2014;Grünwald and Flier 2005;Stukenbrock et al 2007;Vleeshouwers and Oliver 2014;Vleeshouwers et al 2011). Plant pathogens continue to emerge and reemerge and population genetic analyses can be used to infer genetic patterns (subdivision, bottlenecks, clonality, etc.…”

“…Batrachochytrium dendrobatidis, causal agent of the chytridiomycosis pandemic of amphibians, can be traced back to the outbreak of a single clonal lineage (James et al 2009). Yet other pathogens have been shown to emerge via hybridization or speciation (Geiser et al 1998;Giraud et al 2010;Goss et al 2011;Stukenbrock et al 2007). Population genetics can also be useful to provide inferences on the degree of sexual outcrossing by studying linkage among markers (Atallah et al 2010;Goss et al 2014;Milgroom 1996;Milgroom et al 2014).…”