Wild potatoes are native to the Americas, where they present very wide geographical and ecological distribution. Most are diploid, obligate out-crossers due to a multiallelic gametophytic self-incompatibility (S) locus that prevents self-fertilisation and crossing between individuals carrying identical S-alleles. They have two alternative modes of reproduction: sexual (by seeds) and asexual (by stolons and tubers), which provide, respectively, for genetic flexibility in changing environments and high fitness of adapted genotypes under stable conditions. Since the early twentieth century, their taxonomic classification has been mostly based on morphological phenotypes (Taxonomic Species Concept). More recently, attempts have been made to establish phylogenetic relationships, applying molecular tools in samples of populations (accessions) with a previously assigned specific category. However, neither the reproductive biology and breeding relations among spontaneous populations nor the morphological and genetic variability expected in obligate allogamous populations are considered when the taxonomic species concept is applied. In nature, wild potato populations are isolated through external and internal hybridisation barriers; the latter, which are genetically determined, can be either pre-zygotic (pollen-pistil incompatibility) or post-zygotic (abortion of embryo, endosperm or both tissues, sterility, and hybrid weakness and breakdown in segregating generations). The internal barriers, however, can be incomplete, providing opportunities for hybridisation and introgression within and between populations and ploidy levels in areas of overlap. The widespread occurrence of spontaneous hybrids in nature was recognised in the mid-twentieth century. Using genetic approaches, results have been obtained that provide strong support to the assertion that populations are at different stages of genetic divergence and are not at the end of the evolutionary process, as presupposed by the Taxonomic Species Concept. Furthermore, since wild potatoes have uniparental and biparental overlapping generations, the Biological Species Concept - developed for sexually reproducing biparental organisms - cannot be applied to them. In this paper, morphological, genetic, molecular and taxonomic studies in wild potato are reviewed, considering the genetic consequences of their reproductive biology, in an attempt to shed light on the species problem, because of its relevance in germplasm conservation and breeding.
Knowledge of internal hybridization barriers is relevant for germplasm conservation and utilization. The two pre-zygotic barriers are pollen–pistil self-incompatibility (SI) and cross-incompatibility (CI). To ascertain whether SI and CI were phenotypically related phenomena in potatoes, extensive intra- and interspecific, both intra- and interploidy breeding relationships were established, without previous assumptions on the compatibility behavior of the studied germplasm. Pollen–pistil relationships were analyzed at the individual genotype/accession/family level. In two seasons, 828 intra- and interspecific genotypic combinations were performed, using accessions of the wild potatoes Solanum chacoense Bitter (2n = 2x = 24), S. gourlayi Hawkes (2n = 2x = 24; 2n = 4x = 48), and S. spegazzinii Bitter (2n = 2x = 24), full-sibling (hereinafter “full-sib”) families (2n = 2x = 24) within/between the latter two diploids, and S. tuberosum L. (2n = 4x = 48) cultivars. Pollen–pistil incompatibility occurred in the upper first third of the style (I1/3) in all selfed diploids. In both the intra- and interspecific combinations, the most frequent relationship was compatibility, followed by I1/3, but incompatibility also occurred in the stigma and the style (middle third and bottom third). We observed segregation for these relationships in full-sib families, and unilateral and bilateral incompatibility in reciprocal crosses between functional SI genotypes. Cross-incompatibility in potatoes is, apparently, controlled by genes independent of the S-locus or its S-haplotype recognition region (although molecular evidence is needed to confirm it), with segregation even within accessions.
Wild potato species are widely distributed in the Americas, where they spontaneously grow in very diverse habitats. These species - with low chromosome differentiation - form polyploid series with 2n = 2x, 3x, 4x and 6x (x =12). They are isolated in nature by external and internal hybridisation barriers that can be incomplete, allowing hybridisation in areas of sympatry. Nevertheless, most accessions in germplasm banks, regardless of genetic background of the sampled spontaneous populations, have been assigned specific categories based on morphological characters. To further investigate the extent of hybridisation in the group and for comparative purposes, pollen viability was estimated in (i) artificial hybrids between a commercial cultivar (Calén INTA) of the common potato (tetraploid Solanum tuberosum ssp. tuberosum) and the tetraploid cytotype of the related wild species S. gourlayi, and (ii) samples of plants (accessions) and inflorescences of natural populations from Argentina, tentatively classified as 'presumed hybrids' (S. infundibuliforme-S. gourlayi) and 'species' (S. infundibuliforme, S. gourlayi and S. chacoense). Regardless of origin, 98 out of 103 plants analysed had zero to 70% pollen viability (zero to 40% in eight of them). Pollen grains were of variable size and morphology and, in mostly male sterile plants, the only viable pollen grains were 2n and/or 4n. Furthermore, male sterile plants shared various abnormalities in meiosis I and II (unpaired chromosomes, unequal chromosome distribution, precocious/lagging chromosomes, parallel, tripolar, fused and multiple spindles, unequal size nuclei, dyads, triads and pentads in addition to normal tetrads, among others). These results provide novel evidence to support field observations of early potato botanists on the extent of spontaneous hybridisation in wild Argentinian potato populations, which is not reflected in the current taxonomy and has significant consequences for germplasm conservation and breeding.
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