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The first report of the A2 mating (compatibility) type of the potato late blight pathogen, Phytophthora infestans (Mont.) de Bary, outside Mexico was in Europe during 1984 (32) and, since then, the A2 has been found in many parts of the world (19,23). The four most likely hypotheses to explain the occurrence of the A2 mating type outside Mexico are that it (i) was always present, but undetected (58); (ii) was introduced by migration (62); (iii) arose by mutation or mitotic recombination; or (iv) arose by mating type change, either from exposure to fungicides or by induced selfing (39). Among these, the migration hypothesis is the only one with strong scientific support. However, this subject remains somewhat controversial, and alternative explanations for the origin of the A2 mating type of P. infestans outside Mexico still appear occasionally in the literature. Analyses of allozyme data provided the first unambiguous evidence that the A2 mating type in Europe and Japan was introduced by migration from Mexico (62). Numerous additional population genetic studies have fully supported the migration hypothesis (13, 15,18,23,25,40,44,55,63). In each location studied, the first detection of A2 isolates coincided with the appearance of new alleles at allozyme, DNA fingerprint, and mitochondrial DNA loci. Similar changes occurred with the recent appearance of the A2 mating type in the United States (29). Although the detection of new alleles sometimes preceded the A2 (1,25), the A2 never appeared without new alleles (19,23). The migration hypothesis was challenged recently by Ko (39), who proposed instead that mating type change was the origin of the A2 mating type of P. infestans outside Mexico. Ko’s (39) conclusion came from his result that self-fertilization could initiate mating type change. Unfortunately, the mating type change hypothesis in P. infestans was not tested using genetic markers, and no genetic mechanism was proposed by which mating type change could occur. Furthermore, the population genetic data that contradict the mating type change hypothesis were ignored. Part of the proof for the mating type change hypothesis was based on a number of early literature reports that supposedly stated that homothallic isolates of P. infestans were present outside Mexico prior to the 1950s. Unfortunately, these early references were cited without critical evaluation. It is well-known that heterothallic species of Phytophthora produce occasional oospores in single culture (4,21,53,64, 65). It is also quite well documented that oospores of P. infestans were found occasionally during the early part of this century in Europe and the United States (8,48). However, because these structures were produced only rarely and under specific conditions, the scientific consensus was that the sexual stage of P. infestans remained to be discovered. This did not change until the A2 mating type was found in Mexico during the 1950s (21,47,61). Because of the strong evidence for migration, the mating type change hypothesis has never been tested directly. Fortunately, this hypothesis provides testable predictions about the genetic background that should be present in A2 isolates outside Mexico. If the A2 originated by mating type change from A1 mating type populations, the first A2 isolates in each location should be identical, or nearly identical except for mating type, to the previously existing A1 isolates. Sexual reproduction after mating type change could generate new genotypes, but they still should contain only the alleles present in the original A1 populations. Because most populations throughout the world, until recently, were composed primarily, or exclusively, of a single clonal lineage (15,23,25), the mating type change hypothesis is easily testable using molecular markers. Identical multilocus genotypes (or changes limited to a rearrangement of alleles) before and after the occurrence of the A2 mating type would confirm the mating type change hypothesis. In contrast, if the A2 mating type originated by migration, A2 isolates could be similar, or very distinct, from the original A1 isolates, depending on the source population for the migrating genotypes. If the first A2 isolates were very different from isolates in the old A1 populations, the mating type change hypothesis would be rejected. Our purpose was to reanalyze previously published genotypic data to explicitly test the mating type change hypothesis for the origin of the A2 of P. infestans outside Mexico. A secondary goal was to evaluate the early literature to test Ko’s (39) conclusion that homothallic isolates of P. infestans were known outside Mexico prior to the 1950s. Finally, mating type segregations in self-fertilized progenies of P. infestans were analyzed to determine whether mating type change has been observed by other investigators.

Origin of the A2 Mating Type of Phytophthora infestans Outside Mexico