Characterization and acceleration of genome shuffling and ploidy reduction in synthetic allopolyploids by genome sequencing and editing

Abstract

Polyploidy and the subsequent ploidy reduction and genome shuffling are the major driving forces of genome evolution. Here, we revealed short-term allopolyploid genome evolution by sequencing a synthetic intergeneric hybrid (Raphanobrassica, RRCC). In this allotetraploid, the genome deletion was quick, while rearrangement was slow. The core and high-frequency genes tended to be retained while the specific and low-frequency genes tended to be deleted in the hybrid. The large-fragment deletions were enriched in the heterochromatin region and probably derived from chromosome breaks. The intergeneric translocations were primarily of short fragments dependent on homoeology, indicating a gene conversion origin. To accelerate genome shuffling, we developed an efficient genome editing platform for Raphanobrassica. By editing Fanconi Anemia Complementation Group M (FANCM) genes, homoeologous recombination, chromosome deletion and secondary meiosis with additional ploidy reduction were accelerated. FANCM was shown to be a checkpoint of meiosis and controller of ploidy stability. By simultaneously editing FLIP genes, gene conversion was precisely introduced, and mosaic genes were produced around the target site. This intergeneric hybrid and genome editing platform not only provides models that facilitate experimental evolution research by speeding up genome shuffling and conversion but also accelerates plant breeding by enhancing intergeneric genetic exchange and creating new genes.

Patterns, mechanisms, and consequences of homoeologous exchange in allopolyploid angiosperms: a genomic and epigenomic perspective

“…Identifying the HE‐controlling locus (e.g. Ph1 ) and candidate meiotic genes in those regions (Higgins et al ., 2021; Kuo et al ., 2021; Zhang et al ., 2023) in more species would elucidate why certain species have higher rates of HE compared with others. This knowledge could be useful in manipulating recombination in polyploid species and enhancing the practical application of introgression from wild relatives to crop species (Taagen et al ., 2020; Hu et al ., 2021).…”

“…Our understanding of the molecular mechanisms of how HE results in such outcomes remains limited. Characterization of these mechanisms has the capacity to translate directly to the improvement of multiple polyploid crop species due to the integration of HE‐inspired genetic engineering (Zhang et al ., 2023).…”