Genetic Diversity and Origins of the Homoploid-Type Hybrid Phytophthora ×alni

Abstract

Assessing the process that gives rise to hybrid pathogens is central to understanding the evolution of emerging plant diseases. Phytophthora ؋alni, a pathogen of alder, results from the homoploid hybridization of two related species, Phytophthora uniformis and Phytophthora ؋multiformis. Describing the genetic characteristics of P. ؋alni should help us understand how reproductive mechanisms and historical processes shaped the population structure of this emerging hybrid pathogen. The population genetic structure of P. ؋alni and the relationship with its parental species were investigated using 12 microsatellites and one mitochondrial DNA (mtDNA) marker on a European collection of 379 isolates. Populations of P. ؋alni were dominated by one multilocus genotype (MLG). The frequency of this dominant MLG increased after the disease emergence together with a decline in diversity, suggesting that it was favored by a genetic mechanism such as drift or selection. Combined microsatellite and mtDNA results confirmed that P. ؋alni originated from multiple hybridization events that involved different genotypes of the progenitors. Our detailed analyses point to a geographic structure that mirrors that observed for P. uniformis in Europe. The study provides more insights on the contribution of P. uniformis, an invasive species in Europe, to the emergence of Phytophthora-induced alder decline. IMPORTANCEOur study describes an original approach to assess the population genetics of polyploid organisms using microsatellite markers. By studying the parental subgenomes present in the interspecific hybrid P. ؋alni, we were able to assess the geographical and temporal structure of European populations of the hybrid, shedding new light on the evolution of an emerging plant pathogen. In turn, the study of the parental subgenomes permitted us to assess some genetic characteristics of the parental species of P. ؋alni, P. uniformis, and P. ؋multiformis, which are seldom sampled in nature. The subgenomes found in P. ؋alni represent a picture of the "fossilized" diversity of the parental species. Interspecific hybridization can be a rapid track for the evolution of new species in many phylogenetic groups, including fungi and oomycetes (1-3). It has been recognized as an important mechanism of plant disease emergence, with the description of many interspecific hybrid pathogens (4, 5). In particular, in the genus Phytophthora, interspecific hybridization is increasingly seen as a major force generating new taxa: hybrids have been successfully created under laboratory conditions, and more importantly, many natural hybrids have been reported (6-8). Thus, better knowledge of the processes that give rise to hybrid taxa is an important question in the evolutionary biology of emerging pathogens. Understanding the mechanisms that lead to speciation and to the establishment, spread, and evolution of hybrid taxa requires investigation of the identity and genetic variability of parental species and of the directionality and recurrence of the hybr...

Genome-Enhanced Detection and Identification (GEDI) of plant pathogens

“…The possibility to easily obtain multiple alternative regions with equal or improved performance to the ITS region and other universal protein-coding genes commonly used for designing qPCR assays should be of great help in dealing with challenging cases for which higher taxonomic resolution is needed, such as for hybrids and races. Heteroploid organisms such as Phytophthora x alni ( Aguayo et al, 2016 ) represent more complicated cases in the development of qPCR diagnostic tools (e.g., Martin et al, 2012 ). Homology to the putative parental species ( Ioos et al, 2005 ; Inderbitzin et al, 2013 ) and deficiency of concerted evolution in homogenizing intra-individual copies ( Lindner et al, 2013 ) in the ITS region make this marker often unsuitable for assay design in such organisms.…”

Peer Review #1 of "Genome-Enhanced Detection and Identification (GEDI) of plant pathogens (v0.1)"

“…The possibility to easily obtain multiple alternative regions with equal or improved performance to the ITS region and other universal protein-coding genes commonly used for designing qPCR assays should be of great help in dealing with challenging cases for which higher taxonomic resolution is needed, such as for hybrids and races. Heteroploid organisms such as Phytophthora x alni (Aguayo et al, 2016) represent more complicated cases in the development of qPCR diagnostic tools (e.g. Martin et al, 2012).…”

Patterns of Genetic Diversification in the Invasive Hybrid Plant Pathogen Phytophthora × alni and Its Parental Species P. uniformis

“…In a previous study, Aguayo et al [37] evidenced a low polymorphism in P. xalni, with European populations (mainly from France, Germany and Hungary) dominated by a single multilocus genotype (Pxa-1). However, since mtDNA patterns of both parental species were found in P. xalni isolates belonging to the same genotype, the authors concluded that multiple hybridization events occurred independently in several European regions, i.e.…”

“…Subsequent studies showed that the parental species of P. xalni are P. xmultiformis and P. uniformis [34,36]. P. xmultiformis is itself a tetraploid hybrid species which origin is still unknown [34,37]. On the other side, P.…”

“…In this study, we aimed at determining the genetic population structure of P. xalni and P. uniformis in four European countries that were not analyzed by Aguayo et al [37], i.e. Austria, Czech Republic, Lithuania, and Switzerland, and in three previously analyzed countries (Hungary, Spain and Sweden).…”