EU2, a Fourth Evolutionary Lineage of Phytophthora ramorum

Phytophthora ramorum is an aggressive Oomycete pathogen introduced into western North America and western Europe in the late twentieth century by the ornamental plant trade (Goss et al. 2011, Grünwald et al. 2012, Mascheretti et al. 2008, Prospero et al. 2007). The pathogen attacks a wide range of trees and shrubs, causing foliage blights and bleeding stem lesions both in nurseries and in the field (Rizzo et al. 2002, Werres et al. 2001). In North America, P. ramorum is known for causing sudden oak death, the dieback and mortality of millions of coast live oak (Quercus agrifolia Née) and tanoak (Notholithocarpus densiflorus (Hook. & Arn.) Manos, Cannon & S.H. Oh) trees along 1 500 km of near-coastal native forest in California and southwestern Oregon (Grünwald et al. 2008, Rizzo et al. 2002). The pathogen has also spread rapidly and widely across Europe within the nursery trade. From 2003 onwards, it was found attacking rhododendron and some broadleaf trees in the United Kingdom (Brasier et al. 2004) and subsequently native Vaccinium heathlands (P. Beales, Central Science Laboratory, personal communication). Since 2009, P. ramorum has caused sudden larch death, heavy dieback and mortality of plantation Japanese larch (Larix kaempferi (Lam.) Carrière) trees in western Britain and Northern Ireland, resulting in the felling of millions of trees (Brasier and Webber 2010, Webber et al. 2010). Ivors et al. (2006) demonstrated three distinct genetic lineages in P. ramorum. These have since been informally designated NA1, NA2, and EU1 after their initial outbreak locations (Grünwald et al. 2009). NA1 and NA2 are confined to western North America, NA1 being predominant in the forests and found in most nurseries and NA2 so far confined to nurseries and adjacent waterways. Until recently, EU1 was the only lineage found in Europe. EU1 has also been found at a small number of nurseries in the Pacific Northwest. The recent appearance of the lineages is believed to involve independent introduction of NA1 and NA2 into North America and EU1 into Europe; with the appearance of EU1 in North America resulting from a secondary introduction from Europe (Goss et al. 2009a, Goss et al. 2011, Grünwald et al. 2012). All three lineages are near clonal at their presumed centers of introduction, consistent with introduction bottlenecks (Goss et al. 2009b, Grünwald et al. 2008, Ivors et al. 2006, Vercauteren et al. 2010). Significant differences exist among them for important fitness characteristics, such as growth rate, colony stability, and aggressiveness (Brasier et al. 2006a, 2006b; Elliott et al. 2011). Phytophthora ramorum is heterothallic, and to date all NA1 and NA2 lineage isolates have been of A2 sexual compatibility type and EU1 isolates largely of A1 type (Brasier and Kirk 2004, Werres and Kaminski 2005). In Belgium, rare A2s of EU1 lineage have been observed, but these are probably products of somatic recombination from an A1 isolate (Vercauteren et al. 2011b). Gametangial formation between A1s and A2s is unusually sparse and gametangial meiosis often abnormal (Brasier and Kirk 2004, Boutet et al. 2010, Vercauteren et al. 2011a), and a coalescence analysis indicates the lineages may