Key meiotic abnormalities impair pollen viability in aneuploid Brassica napus

Aneuploidy, frequently observed in plants, is an evolutionary intermediate that plays a key role in speciation and phenotypic diversification. However, the effect of meiosis on pollen viability in aneuploids remains elusive. Herein, we studied chromosome inheritance patterns of aneuploids with complex karyotypes by investigating the pairing and segregation behavior of each chromosome at diakinesis and anaphase I during meiosis in Brassica napus. In aneuploids, we observed distinct chromosome behaviors: (1) tetrasomic chromosomes primarily formed quadrivalents or two independent bivalents and showed equal segregation; (2) trisomic chromosomes exhibited mixed trivalent/bivalent-univalent pairing with exclusively 1:2 segregation; (3) disomic chromosomes displayed basically normal chromosome pairing and equal segregation; (4) monosomic chromosomes remained predominantly as a univalent and showed random segregation. Primary meiotic pairing abnormalities, including nonhomologous associations of homoeologs and 45S rDNA loci at diakinesis, were identified. Homologous nondisjunction was the most prevalent abnormality during meiotic anaphase I, and pollen viability and chromosomal aberrations were negatively correlated at this stage. Aneuploids of B. napus complete meiosis successfully, generating viable aneuploid male gametes. Our study provides fundamental insights into chromosome inheritance in aneuploids and can shed light on the cytogenetic basis of partial pollen viability in plant aneuploids.