The Population Structure of Phytophthora infestans from the Toluca Valley of Central Mexico Suggests Genetic Differentiation Between Populations from Cultivated Potato and Wild Solanum spp.

Abstract

The population structure of Phytophthora infestans in the Toluca Valley of central Mexico was assessed using 170 isolates collected from cultivated potatoes and the native wild Solanum spp., S. demissum and S. xendinense. All isolates were analyzed for mitochondrial DNA (mtDNA) haplotype and amplified fragment length polymorphism (AFLP) multi-locus fingerprint genotype. Isolate samples were monomorphic for mtDNA haplotype because all isolates tested were of the Ia haplotype. A total of 158 multilocus AFLP genotypes were identified among the 170 P. infestans isolates included in this study. P. infestans populations sampled in the Toluca Valley in 1997 were highly variable and almost every single isolate represented a unique genotype based on the analysis of 165 AFLP marker loci. Populations of P. infestans collected from the commercial potato-growing region in the valley, the subsistence potato production area along the slopes of the Nevado de Toluca, and the native Solanum spp. on the forested slopes of the volcano showed a high degree of genetic diversity. The number of polymorphic loci varied from 20.0 to 62.4% for isolates collected from the field station and wild Solanum spp. On average, 81.8% (135) of the AFLP loci were polymorphic. Hetero-zygosity varied between 7.7 and 19.4%. Significant differentiation was found at the population level between strains originating from cultivated potatoes and wild Solanum spp. (P = 0.001 to 0.022). Private alleles were observed in individual isolates collected from all three populations, with numbers of unique dominant alleles varying from 9 to 16 for isolates collected from commercial potato crops and native Solanum spp., respectively. Four AFLP markers were exclusively found present in isolates collected from S. demissum. Indirect estimation of gene flow between populations indicated restricted gene flow between both P. infestans populations from cultivated potatoes and wild Solanum hosts. There was no evidence found for the presence of substructuring at the subpopulation (field) level. We hypothesize that population differentiation and genetic isolation of P. infestans in the Toluca Valley is driven by host-specific factors (i.e., R-genes) widely distributed in wild Solanum spp. and random genetic drift.

An Andean origin of Phytophthora infestans inferred from mitochondrial and nuclear gene genealogies

“…2), as has been observed by others using different molecular markers (23,24). The two most common nuclear haplotypes (H1 and H2) of each ancient lineage contained isolates of both mtDNA lineages (types I and II) and of both mating types (A1 and A2).…”

“…One possible mechanism might be that domestic potatoes provide a different environment and therefore selected different mtDNA haplotypes than wild Solanum species (23,24). However, so far the same mtDNA haplotype (type Ia) has been found associated with both wild and cultivated potatoes in Toluca (24). No indication of selection in either mitochondrial or nuclear loci for the Mexican population or the pooled sample was found (SI Table 2).…”

“…Selection has been proposed to explain the presence of only one mtDNA haplotype (type Ia) of P. infestans in Toluca Mexico (18). One possible mechanism might be that domestic potatoes provide a different environment and therefore selected different mtDNA haplotypes than wild Solanum species (23,24). However, so far the same mtDNA haplotype (type Ia) has been found associated with both wild and cultivated potatoes in Toluca (24).…”

“…Greater diversity in a place may be due to a particular history of founder effects, extinctions, and expansions of local populations. In contrast, there is less mitochondrial diversity in Toluca Mexico and the predominance of one maternal lineage suggests either a single maternal origin for this population or selection (23,24). The mitochondrial genome is inherited maternally as a unit in P. infestans, without genetic recombination (23).…”

“…Spread of a single clonal lineage, the US-1 (Ib mtDNA haplotype) was proposed (4). The US-1 lineage is not found widely in extant Mexican populations of P. infestans (12,23,24), whereas this lineage is still found in other populations around the world including the Andes. We sequenced the mtDNA from historic specimens of P. infestans from the Irish famine and found the Ia haplotype was common (25,26).…”