Genomic insights into biased allele loss and increased gene numbers after genome duplication in autotetraploid Cyclocarya paliurus

Background Autopolyploidy is a valuable model for studying whole-genome duplication (WGD) without hybridization, yet little is known about the genomic structural and functional changes that occur in autopolyploids after WGD. Cyclocarya paliurus (Juglandaceae) is a natural diploid-autotetraploid species. We generated an allele-aware auto-tetraploid genome, a chimeric chromosome-level diploid genome, and whole-genome resequencing data for 106 autotetraploid individuals at an average depth of 60 x per individual, along with 12 diploid individuals at an average depth of 90 x per individual. Results Autotetraploid C. paliurus had 64 chromosomes clustered into 16 homologous groups, and the majority of homologous chromosomes demonstrated similar chromosome length, gene numbers, and expression. The regions of synteny, structural variation and nonalignment to the diploid genome accounted for 81.3%, 8.8% and 9.9% of the autotetraploid genome, respectively. Our analyses identified 20,626 genes (69.18%) with four alleles and 9191 genes (30.82%) with one, two, or three alleles, suggesting post-polyploid allelic loss. Genes with allelic loss were found to occur more often in proximity to or within structural variations and exhibited a marked overlap with transposable elements. Additionally, such genes showed a reduced tendency to interact with other genes. We also found 102 genes with more than four copies in the autotetraploid genome, and their expression levels were significantly higher than their diploid counterparts. These genes were enriched in enzymes involved in stress response and plant defense, potentially contributing to the evolutionary success of autotetraploids. Our population genomic analyses suggested a single origin of autotetraploids and recent divergence (similar to 0.57 Mya) from diploids, with minimal interploidy admixture. Conclusions Our results indicate the potential for genomic and functional reorganization, which may contribute to evolutionary success in autotetraploid C. paliurus.

Automated summary

Background: Autopolyploidy is a valuable model for studying whole-genome duplication without hybridization, yet little is known about the genomic structural and functional changes that occur in autopolyploids after duplication. In this study, we investigated these changes in Cyclocarya paliurus, a natural diploid-autotetraploid species. Results: The autotetraploid C. paliurus had 64 chromosomes clustered into 16 homologous groups, and most of these homologous chromosomes showed similar characteristics. The genomic regions of synteny, structural variation, and nonalignment to the diploid genome accounted for different proportions of the autotetraploid genome. Moreover, we found that genes with allelic loss were often located near structural variations and transposable elements, and these genes showed reduced interaction with other genes. Furthermore, we identified genes with more than four copies in the autotetraploid genome, and these genes exhibited higher expression levels than their diploid counterparts. These genes were involved in stress response and plant defense, suggesting their role in the evolutionary success of autotetraploids. Population genomic analyses revealed a single origin of autotetraploids and recent divergence from diploids. Conclusions: Our findings indicate the potential for genomic and functional reorganization in autotetraploid C. paliurus, which may contribute to their evolutionary success.