Chromosome pairing during meiosis in Brassica hybrid allodiploids with evolutionarily related genomes

Varying rates in chromosome pairing, chromosomal fragmentation and chromosome loss during meiosis, indicates homologous recombination pathway of DNA damage repair was challenged to different degrees in three Brassica hybrid allodiploids. Sequence similarity of combined genomes in plant hybrid species can shape chromosome pairing and synapsis during meiosis, but the extent remains unclear. The present study investigated meiotic chromosomal behaviors in three typical Brassica hybrid allodiploids (AB, AC and BC) as models with the evolutionarily related genomes from B. rapa (AA), B. nigra (BB) and B. oleracea (CC). The results showed that chromosome allosyndesis occurred at the pachytene with the varying rate and led to different frequencies of univalents, bivalents, and multivalents, and finally caused the imbalanced segregation with retard chromosomes in daughter cells during meiosis in allodiploids AB, AC and BC. Notably, allodiploid AC displayed an increased incidence of bivalent formation, chromosome bridges, and chromosomal fragmentation. Conversely, allodiploid BC was prone to chromosome loss, particularly within the C genome, and exhibited the highest frequency of lagging chromosomes, resulting in micronuclei and spindle disarray. Transcriptomic analysis revealed that in allodiploid AC the up-regulated genes were predominantly involved in synapsis (ASY1, RBR1), microtubule assembly (AUG4, AUG5, AUG6), and DNA damage repair (BRCA1, BRCA2, FAS1) pathways. In contrast, genes related to DNA damage repair (PMS1, LIG4, ALT2) were mostly transcription-deficient in allodiploids AB and BC, predisposing these hybrids to extensive DNA damage and chromosome lag. Collectively, these findings underscore the profound impact of genomic combinations with sequence divergence on chromosom pairing during meiosis in plant hybrid species.