Author's personal copy Evolutionary history of the mitochondrial genome in Mycosphaerella populations infecting bread wheat, durum wheat and wild grasses Stefano F.F. Torriani ⇑ , Patrick C. Brunner, Bruce A. McDonald Plant Pathology Group, Institute of Integrative Biology, ETH Zurich, CH-8092 Zurich, Switzerland article info Article history: Received 12 May 2010 Revised 10 November 2010 Accepted 2 December 2010 Available online 9 December 2010 Keywords: mtDNA Selective sweep Septoria tritici Triticum aestivum Triticum durum abstract Plant pathogens emerge in agro-ecosystems following different evolutionary mechanisms over different time scales. Previous analyses based on sequence variation at six nuclear loci indicated that Mycosphaerella graminicola diverged from an ancestral population adapted to wild grasses during the process of wheat domestication approximately 10,500 years ago. We tested this hypothesis by conducting coalescence analyses based on four mitochondrial loci using 143 isolates that included four closely related pathogen species originating from four continents. Pathogen isolates from bread and durum wheat were included to evaluate the emergence of specificity towards these hosts in M. graminicola. Although mitochondrial and nuclear genomes differed greatly in degree of genetic variability, their coalescence was remarkably con- gruent, supporting the proposed origin of M. graminicola through host tracking. The coalescence analysis was unable to trace M. graminicola host specificity through recent evolutionary time, indicating that the specificity towards durum or bread wheat emerged following the domestication of the pathogen on wheat. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction Archeological findings (Childe, 1953; Gopher et al., 2002; Moore et al., 2000) and genetic studies (Salamini et al., 2002) place the origins of agriculture in the Fertile Crescent of the Middle East be- tween 10,000 and 12,000 years ago. The wild progenitors of the major Neolithic founder crops including wheat (Triticum spp.), bar- ley (Hordeum vulgare) and pea (Pisum sativum) have been identified in this region (Diamond, 1997; Haudry et al., 2007). The domestica- tion of wild grasses is thought to have been a slow process reflecting the gradual selection of desired agronomic traits, including in- creased seed size, stiffness of the ear rachis and easy release of the seed (Elias et al., 1996; Sharma and Waines, 1980; Taenzler et al., 2002). Natural ecosystems were transformed into agro-ecosystems during the spread of agriculture (Stukenbrock and McDonald, 2008). The impact of agricultural practices on the emergence of crop pathogens can be inferred by dating the divergence time between pathogens on cultivated crops and their progenitors on wild plants. The few studies that have followed this approach have utilized nu- clear genes in plant pathogenic fungi (Couch et al., 2005; Munkacsi et al., 2008; Stukenbrock et al., 2007; Zaffarano et al., 2008). Based on detailed analyses of six nuclear loci, Stukenbrock et al. (2007) pro- posed that Mycosphaerella graminicola emerged as a wheat pathogen from ancestral populations of Mycosphaerella spp. (called S1 and S2) infecting wild grasses in the Middle East during the process of wheat domestication around 10,500 years ago. Other studies indicated that M. graminicola became distributed throughout Europe during the spread of wheat cultivation approximately 5000–8000 years ago (Banke et al., 2004; McDonald et al., 1999) and more recently (500 and 150 years ago, respectively) was introduced into the New World by European colonists who brought wheat into the Americas and Australia (Banke and McDonald, 2005). M. graminicola is one of the most important foliar pathogens of wheat and occurs across a wide range of climates (Eyal, 1999; Polley and Thomas, 1991). The life cycle includes both sexual and asexual stages, with the wind dispersed sexual ascospores having the potential to move several kilometers (Sanderson, 1972) while the asexual pycnidiospores are disseminated via rain-splash over distances of only a few meters (Bannon and Cooke, 1998). M. graminicola populations around the world are characterized by high nuclear and low mitochondrial (mt) diversity (Zhan et al., 2003). High gene flow (Boeger et al., 1993) coupled with large effective population sizes (Zhan and McDonald, 2004) and recur- ring sexual reproduction give rise to the high observed nuclear diversity (Chen and McDonald, 1996; Hunter et al., 1999). In con- trast, Zhan et al. (2003) identified only seven mtRFLP haplotypes among a global collection of 1673 isolates, with the two most fre- quent (type 1 and type 3) found in approximately 93% of all tested isolates. Restriction mapping showed that differences among mtRFLP haplotypes were mainly insertion or deletion polymor- phisms (indels). Among the same 1673 strains, 1327 distinct nuclear genotypes were reported. Based on comparison of entire 1055-7903/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2010.12.002 ⇑ Corresponding author. Address: Plant Pathology Group, ETH Zurich/LFWA27, Universitätstrasse 2, CH-8092 Zurich, Switzerland. Fax: +41 (0) 44 632 1572. E-mail address: stefano.torriani@agrl.ethz.ch (S.F.F. Torriani). Molecular Phylogenetics and Evolution 58 (2011) 192–197 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev