Promiscuous potatoes: the genetic basis of wild potato compatibility

Abstract

Few plants have shaped dinner plates and world history quite like the potato. Both the tetraploid cultivated potato (Solanum tuberosum L.) and its wild tuber-bearing relatives belong phylogenetically to the Solanum section Petota (Yan et al., 2023). There are more than 100 recognized species of cultivated potatoes and their wild relatives. Like cultivated potatoes, many of these carry the A genome; they are primarily found in South America and are reproductively isolated from Mexican diploid species. The only diploid A-genome species occurring in Mexico is Solanum verrucosum Schlechtendal, which also serves as a maternal ancestor of Mexican polyploid species (Hosaka et al., 2022). Interestingly, S. verrucosum is also the only A-genome diploid potato species that is fully self-compatible.

William Behling, first author of the highlighted publication, has long been fascinated by crop wild relatives, and he was especially drawn to S. verrucosum, which can serve as a bridge between the gene pool of cultivated and wild species because it can be fertilized by a broad range of wild Solanum species (Behling et al., 2024). The more he worked with S. verrucosum, the more he wanted to know why this species was able to do something that no other potato species seemed to be able to do—accept pollen from any male-fertile pollen donor.

In S. verrucosum, self-compatibility has been attributed to the lack of S-ribonuclease (S-RNase) expression in the style (Eijlander et al., 2000). Together with other factors such as HT genes, the S-RNase has a cytotoxic effect on incompatible pollen tubes penetrating the style. However, knocking out the S-RNase gene in S. tuberosum is not sufficient to replicate the phenotypes observed in S. verrucosum (Behling & Douches, 2023). Additionally, there are examples of pollen rejection mechanisms that are independent of S-RNase in interspecific pollinations in tomato (Tovar-Méndez et al., 2017). Therefore, Behling, David Douches and colleagues set out to identify additional genetic factors that determine interspecific compatibility in S. verrucosum (Behling et al., 2025).

To create a F2 mapping population, segregating for the presence and absence of interspecific reproductive barriers (IRBs), the authors selected two Solanum parents differing in their reproductive behaviour: DM1S1, a S. tuberosum doubled monoploid that is effectively male sterile and has functional IRBs, but is able to accept pollen from S. verrucosum; and MSJJ1813-2, a S. verrucosum clonal selection that exhibits a high degree of male fertility, self-compatibility and lacks IRBs (Figure 1a).

To test for self-compatibility, the population was then allowed to self-pollinate. The authors first classified the phenotypes as self-compatible or self-incompatible. However, they found that the group of F2 progeny that they initially classified as self-incompatible produced pollen that was not germinating on the styles in self-pollinations and failed to germinate in vitro, indicating that these plants were male sterile. To test for interspecific compatibility, the F2 was pollinated with pollen of S. pinnatisectum or of S. tarnii because these species have strong IRBs with S. tuberosum (Figure 1b). As a result of the interspecific crosses, the phenotypes were classified as functional IRBs or lacking IRBs.

Then, the authors performed single nucleotide polymorphism (SNP) genotyping, created a linkage map and performed quantitative trait locus (QTL) analysis. They identified two regions associated with interspecific compatibility on Chromosomes 1 and 11. The region on Chromosome 1 encompassed the centromeric region, as previously reported (Hosaka et al., 2022), and the S-locus, again confirming there are more mechanisms than just the presence or absence of S-RNase. Three QTLs were associated with male fertility, with significant SNPs located close to genes encoding phospholipid:diacylglycerol acyltransferases, UDP-glycosyltransferase superfamily proteins, pectinacetylesterase family proteins and receptor lectin kinases, all previously associated with pollen development and fertility (Bai et al., 2023).

On Chromosomes 1, 6, 8 and 11, the authors observed transmission ratio distortion (TRD), meaning that alleles did not segregate according to the expected Mendelian ratios. Two loci showing TRD were linked to reproductive traits: the S-locus on Chromosome 1, which harbours the S-RNase gene and controls self-compatibility, and a locus on Chromosome 8 associated with male fertility. At the S-locus, TRD was expected because of the self-incompatibility mechanism: Pollen tubes carrying the same S-allele as the pistil are actively blocked from reaching the ovary, preventing that allele from being transmitted.

Fine-mapping of the QTL on Chromosome 1 proved challenging because recombination is suppressed in the pericentromeric region. Furthermore, the S-locus mediates gametophytic self-incompatibility in DM1S1, leading to strong prezygotic selection against DM1S1 S-alleles. To gain more insight into the region on Chromosome 1, the authors performed RNA sequencing of styles and pollen from both parents of the F2 population and from three F2 individuals representing the range of phenotypic variation. Differential gene expression analysis was conducted by comparing stylar transcriptomes of F2 individuals to both parents, then filtering results to the QTL region. Notably, S-RNase was among the candidates: In some F2 plants, S-RNase expression was absent, as in MSII1813-2, while it was present in others. Interestingly, F2 progeny with either functional or non-functional IRB shared S-RNase expression profiles with S. verrucosum yet exhibited different phenotypes. This expression pattern again indicates that, in addition to the S-locus on Chromosome 1, the QTL on Chromosome 11 also contributes to IRB function.

Within the QTL on Chromosome 11, the authors identified a candidate gene whose expression correlated with the ability to accept interspecific pollen: a gene encoding a fatty acyl-CoA reductase. The role of fatty acyl-CoA reductases is well-established in male fertility (Zhang et al., 2022), but their role in interspecific reproductive barriers had not previously been described. The authors propose that this gene might participate in direct or indirect signalling between growing pollen tubes and the style.

Elucidating the genetic basis of IRB is a critical next step towards the broader objective of Douches' research group: introgressing economically important traits from wild species into cultivated potato. Breeders could leverage S. verrucosum or its derivatives to access the vast genetic resources of wild potato species, which harbour a wealth of additional traits for disease and pest resistance (Bethke et al., 2017).