Chromosomal and haplotypic biased genomic instability in the autotetraploid potato cultivar C88

Cultivated potato (Solanum tuberosum) is an autotetraploid crop whose tetrasomic inheritance and highly heterozygous genome constrain breeding efficiency. Although previous studies have generally reported genome instability in cultivated potatoes, the underlying mechanisms remain insufficiently understood. Genomic inheritance and variation were investigated by integrating oligo-fluorescence in situ hybridization (FISH) cytogenetic observation, population genomics analysis and haplotype genetic tracking in the autotetraploid potato C88 and its selfing progeny population of 1,034 lines. During parental meiosis in C88, abnormal chromosomal configuration (1II+2I) at diakinesis significantly correlated with premature sister chromatid separation (PSCS) at anaphase I. This meiotic abnormality directly causes widespread genome instability in the progeny, resulting in elevated aneuploidy frequency. Chromosome 11 showed the highest loss rate (4.16%), indicating biased chromosomal instability. Among 1,034 selfing progeny, duplication copy number variations exceeded deletions. Haplotype genetic analysis of progeny with chromosome 11 aneuploidy revealed predominant transmission from parental H1 and H3 haplotypes, suggesting strong homologous pairing preference and non-random transmission. Our findings suggest a mechanism linking abnormal meiosis in the C88 parent to biased genome instability in its selfing progeny, providing a framework for future studies on polyploid genome instability and breeding.