The structure and allelic diversity of the self-incompatibility locus (S-locus) in diploid potatoes inferred from whole genome sequences and transcriptome data from styles and pollen

Authors: AMES, MERCEDES - University Of Wisconsin; Halterman, Dennis; Bethke, Paul

Submitted to: The Plant Genome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/7/2025
Publication Date: 11/10/2025
Citation: Ames, M., Halterman, D.A., Bethke, P.C. 2025. The structure and allelic diversity of the self-incompatibility locus (S-locus) in diploid potatoes inferred from whole genome sequences and transcriptome data from styles and pollen. The Plant Genome. https://doi.org/10.22541/essoar.176278171.10448063/v1.
DOI: https://doi.org/10.22541/essoar.176278171.10448063/v1

Interpretive Summary: Gametophytic self-incompatibility is a reproductive strategy to prevent inbreeding and promote outcrossing. Studies to understand molecular and evolutionary aspects of the self-incompatibility/self-compatibility system in the Solanaceae have been conducted using several genera including Petunia, Nicotiana, and Solanum. Interest in converting potato from a tetraploid (4x), vegetatively propagated crop to a diploid (2x) inbred-hybrid crop has highlighted the need to better understand the self-incompatibility system in potato and wild species relatives of potatoes, most of which are diploid and self-incompatible. It is well known that S-locus RNases (S-RNases) are the pistil determinant of gametophytic self-incompatibility and multiple S-RNase alleles have been identified in a few potato species. It is also known that the pollen determinants of self-incompatibility are S-locus F-box proteins (SLFs) that are likely linked to S-RNases on chromosome 1. The S-RNase and SLFs present on each chromatid determine an individual’s compatible/incompatible haplotypes. However, the extent of SLF diversity, the number and position of SLFs in the S-locus, and the mechanism of interaction between SLFs and S-RNases is unknown in potatoes. A combination of genome sequencing and analysis of transcriptomes from pollen and pistils of wild and cultivated diploid potatoes was used to determine the structure of the S-locus. Our analysis showed that SLF sequences are expressed in pollen but not in styles, vary in number between individuals, and are distributed across a 10-15 Mb region that typically contains one S-RNase gene. This is the first detailed description of female and male components in S-locus haplotypes. This research may shed light on how these two pistil and pollen elements interact to determine self-compatibility or incompatibility and may further our understanding of gene flow in wild Solanum species.

Technical Abstract: Some plants, including members of the potato family, have a natural system that prevents self-pollination. This mechanism helps plants to stay naturally competitive by preventing harmful inbreeding. Plant breeders, however, use selective inbreeding to produce superior crops, such as hybrid corn. There is growing interest in using inbreeding and hybridization as tools for potato breeding. Our study focused on two key genes, S-RNase genes and SLF genes, that control whether a potato plant can self-pollinate or not. These genes function in two places in a potato plant. S-RNases act in the part of the flower that receives pollen (the pistil) and SLFs act in the pollen. Pollination is prevented when the S-RNases and SLFs don't "match" correctly. We used data from wild and cultivated potato plants to determine where these genes are located in potato DNA and how they work. We found that SLF genes are only active in pollen, vary widely among different plants, and are spread out over a large section of one chromosome near the S-RNase gene. This is the first detailed look at how the genes from the pistil and the pollen work together in potatoes to control self-pollination. Understanding this system could help scientists develop better potato breeding methods and learn more about how genetic changes occur over time in wild potato populations.